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Evaluation methods of sagittal curvatures in invasive examinations of the spine: a systematic review

Introdução: A avaliação das curvaturas sagitais da coluna vertebral auxilia na determinação dos padrões posturais dos indivíduos. Objetivo: Revisar sistematicamente os métodos de avaliação das curvaturas sagitais da coluna vertebral no exame de Raios-X descritos em estudos observacionais. Métodos: Foi realizada uma busca sistemática nas bases de dados Scopus, Science, Bireme e Pubmed. Os principais desfechos extraídos foram os métodos utilizados para avaliar as curvaturas torácica e lombar da coluna vertebral no plano sagital através do exame de Raios-X. Para avaliação da qualidade metodológica foi utilizado o checklist de Brink&, Louw. Resultados: Nos 23 artigos incluídos nessa revisão, encontramos nove métodos diferentes para avaliar as curvaturas sagitais, tais como Cobb (2 ou 4 linhas), Cobb alternativo, Cobb máximo ou não constricto, Raio da curvatura, TRALL, Círculos tangenciais, Tangentes posteriores, Centroides e PR. Os métodos não dependentes dos platôs vertebrais, tais como Centroides, Círculos tangenciais, Cobb alternativo, Raio da curvatura para a coluna torácica; Centroide, Tangente posterior, TRALL e PR para a lombar apresentam iguais ou melhores valores de reprodutibilidade e menor variabilidade de medidas que quando comparados ao ângulo Cobb. Conclusão: Os métodos encontrados mostraram grande correlação com o padrão ouro (ângulo Cobb), tanto para coluna torácica, quanto para a lombar, e podem ser utilizados, em ambos os âmbitos, da pesquisa e da prática clínica, já que apresentam iguais ou melhores valores de reprodutibilidade e menor variabilidade de medidas que quando comparados ao ângulo Cobb.


INTRODUCTION
The assessment of sagittal spinal curvatures assists in determining postural patterns of individuals (Čelan et al., 2012). The gold standard for such evaluations are the X-ray examinations lateral-lateral (Zaina et al., 2003) in which the calculations of the Cobb angles are performed, able to quantify the magnitude of these curvatures (Briggs et al., 2007).
However, many critical regarding the Cobb method are described in literature, such as the difficulty in selecting the endplate of the cranial and caudal vertebrae to perform mensuration (Harrison, Harrison, et al., 2001). Another major criticism of this method is the fact that this measure allows only the final information of the curve without knowledge of the segments involved (Harrison, Harrison, et al., 2001) . Besides, to calculate the angle of traditional Cobb method the formation of the four lines is required, being the high amount of intra-and inter-observer error (5-10 degrees) another potential source of criticism to the method (Carman et al., 1990).
These criticisms may have encouraged the development of alternatives to a segmental analysis or other ways of evaluating the sagittal plane of the radiographs, such as the tangent of the posterior vertebral bodies (Bernhardt e Bridwell, 1989), methods using the centroid of vertebrae (Harrison, Donald D et al., 1998;Chen, 1999) and TRALL (Chernukha et al., 1998) method.
Although these methods are well described in the literature, we did not find information on which one of them have lower variability and higher reliability of the measures. Thus, the aim of this study is to systematically review the methods of evaluation of sagittal curvatures of the spine in examining X-rays of children, adolescents, adults and elderly, healthy, with or without postural changes described in observational studies. It is expected that the results of this systematic review may help health-care professionals in choosing the most appropriate method to evaluate with greater accuracy and reliability the sagittal curvatures of the spine in X-rays examinations.

METHODOLOGY
This review follows the recommendations suggested by the Collaboration Cochrane (Higgins e Green, 2011), with observational studies as eligibility criteria, showing the radiographic evaluation in the sagittal plane of the thoracic and lumbar curvatures of the spine in children, adolescents, adults and elderly, healthy, with or without postural changes, written in English. Therefore, a systematic research was conducted in Scopus databases, Science, Bireme and Pubmed in August 2015.
The keywords used were: "Validation Studies" [Publication Type] OR "Reproducibility of Results" [Mesh]" AND

" T h o r a c i c Ve r t e b r a e " [ M e s h ] O R " L u m b a r
Vertebrae" [Mesh] AND "Radiography" [Mesh] AND "Adolescent" [Mesh] OR "Young Adult" [Mesh] OR "Adult" [Mesh] OR "Aged" [Mesh] OR "Elderly" [All Fields] OR "Humans" [Mesh] OR "Human" [All Fields] OR "Child" [Mesh] AND "Kyphosis" [Mesh] OR "Lordosis" [Mesh] OR "sagittal" OR "lateral".
Initially, the studies were selected from reading the titles and abstracts, and articles that had the potential to be included in the research were read and analyzed in full. Afterwards, those who fulfilled all inclusion criteria were finally included. The references of each article included were also investigated in order to find articles not located in the electronic research. All the research procedures, selection, evaluation of quality, data extraction and reading of the articles were performed by two independent evaluators. In case of divergence of views among evaluators, a third evaluator was invited to conduct the evaluation of the article.
The two researchers evaluated independently the full articles included in the review and the extraction of data occurred through a standardized form. The main outcomes from the studies were methods used to evaluate the thoracic and lumbar curvatures of the spine in the sagittal plane through X-rays examinations. Other outcomes were: average value, standard deviation, average differences between measurements, intra-and inter-observer reliability analysis. In case of disagreement among researchers regarding the data derived from studies, it was resolved by consensus between them or by consulting a third more experienced researcher. While the study did not show all the necessary data for the review, the corresponding author was contacted to request the missing data.
To evaluate the methodological quality a checklist proposed by Brink &, Louw(Brink et al., 2011) (2011 was used, which was designed to test the reliability and validity studies. This tool consists of 13 items and it was developed from two scales, the Quality Assessment of Diagnostic Accuracy Studies (QUADAS) and the Quality Appraisal of Diagnostic Reliability Studies (QAREL). The studies were considered high quality if they had a ≥ 60% (up to 8) score in the applicable items, according to prior use in other works of the same type (May et al., 2010;Adhia et al., 2013). Two reviewers independently evaluated the methodological quality of the included studies.
Any disagreement was discussed between them and whenever the disagreement persisted, a third reviewer was consulted.
Considering the divergence of terminology between the studies, for the validation criteria of the instruments and for facilitating the comparison between the results, the terminology has been standardized in this systematic review as follows: the repeatability was considered as the degree of agreement obtained from evaluations performed on successive instants by the same evalua-tor; intra-rater reproducibility as the degree of reproducibility of the measurements performed by the same rater, varying the time between the collection (with a minimum interval of one day); inter-rater reproducibility and the degree of reproducibility of the measurements made by different observers; and concurrent validity as the agreement between the instrument under test and the instrument considered the gold standard for variable evaluation study (Bipm et al., 2008).

RESULTS
Initially 1583 articles were found, of these, 278 were excluded because they were duplicates and 1254 did not meet the inclusion criteria. Thus, 51 studies were initially included in this systematic review. After reading in full, 22 studies met the inclusion criteria. Subsequently, their references were analyzed and one more article was added to subsequent data extraction ( Figure 1).  Table 1 shows the evaluation of methodological quality used in this systematic review. Of the 22 studies selected, only two were classified as being of low quality, and, thus, weak scientific evidence.
Criteria QUADAS and QAREL: 1. Appropriate description of the sample; 2. Adequate description of the evaluators; 3. Adequate explanation of the reference standard; 4. Blinding inter evaluators; 5. Blinding intra evaluators; 6. evaluation order of variation; 7. Length of time between the rated test and the reference standard; 8. Length of time between repeated measurements; 9. benchmark Independence of the evaluated test; 10. Adequate description of the evaluated test procedure; 11. Adequate description of the benchmark of the procedure; 12. Explanation of any sample loss; 13. Appropriate statistical methods. Answers to the criteria: Y=Yes; N=No; N/A= Not Applicable.
Average of differences between intra-and inter-rater = close to zero.
Average and standard deviation of Difference between measures varied from 0,1º to 0,5º with the standard deviation of 2,26º.
n=20, average age of 46 years old.
PR-L1. Test t did not show differences between measurements.
posterior Tangent  In the studies that reported data on the reproduci-

bility, the ICC values (Intraclass Correlation Coefficient)
intra-and inter-rater were higher than 0.75, which according to Shrout, Fleiss(Shrout e Fleiss, 1979) (1986 are considered excellent (Jackson et al., 1998b;Harrison, Harrison, et al., 2001;Gardocki et al., 2002;Briggs et al., 2007). The exceptions were the studies of Jackson (2000) (Jackson et al., 2000a) and Mac Thiong (2007) ( Mac-Thiong et al., 2007), who found an intra-rater ICC of 0.63 and 0.74 for Cobb T1-T12. The authors report that the greatest difficulty is the T1 scanning, attributing the lower reproducibility of the overlapping shoulders in X-ray examinations, making it difficult to identify and scan of the plateaus T1 vertebra in X-Ray images (Jackson et al., 2000a;Mac-Thiong et al., 2007). Therefore, the SEM value is also an indication of the reproducibility of measure, this is, the lower the SEM is the more reproducible is the method analyzed. Briggs (2007) (Briggs et al., 2007) was the only study which presented these values, being the higher SEM that one which refers to the inter-rater reproducibility of the Cobb angle T1-T12 (4º).
Concerning the measure values and standard deviation (SD), the Cobb T1-T12 and constricted Cobb showed higher DP values when compared, respectively, to the Centroid method T1-T12 (Briggs et al., 2007) and not constricted Cobb (Mac-Thiong et al., 2007). It is worth mentioning that, the lower the standard deviation is, the lower the variability of the measure is, therefore, combined with other aspects concerning the measures, it is essential that also such values are also analyzed in order to identify what is the most appropriate method to be used in clinical practice and scientific research.
The Cobb method is very sensitive to changes in contour and concavity and degeneration of plateaus, so it may show some mistakes which tend to overestimate the value of the curvature. This can be identified, for example, in the evaluation of the thoracic kyphosis in the population with osteoporosis or with Scheuermann disease, whose vertebrae are shown in wedge shape; or in cases of vertebral fractures, in which the selection of the terminal vertebra is inconsistent, and there is great difficulty in identifying the plateausterminal (Troyanovich et al., 1998;Chen, 1999;Goh et al., 2000;Harrison, Harrison, et al., 2001;Briggs et al., 2007;Hong et al., 2010). Moreover, in the calculation of T1-T12 Cobb angle, errors may come because of the impaired view, particularly in too brightimages (Briggs et al., 2007), so, most often other vertebral limits are chosen.
Also in this idea,  believes that the Cobb method does not have the capacity to evaluate the real global curvature because it determines fixed vertebrae as their levels to the angulation. In an attempt to correct this limitation, the authors used the maximum Cobb for comparison with the tangential circles. This method, on the other hand, provides a geometric model based on the curvature as a whole, apart from that is not influenced by the architecture of the plateaus or intervertebral discs. Another advantage is the visualization in radiographic images, particularly in the thoracic spine in the anterior part of vertebral bodies is more easily visible, a fact which contributes to better reproducibility (Hong et al., 2010) values. Chen (1999) (Chen, 1999) reports that the superiority of the Centroid is the use of four vertebrae for the angulation, not being dependent on the plateaus, which increases the reproducibility of the method in question (Harrison, D. D. et al., 1998), corroborating Briggs (2007) (Briggs et al., 2007), who reaffirms this benefit in his work and justifies the use of the Centroid in people with kyphosis above 58,25º being, therefore, an advantageous alternative for people with osteoporosis.
Regarding the studies that tested the concurrent validity of data between a new method and Cobb (Goh et al., 2000;Briggs et al., 2007;Mac-Thiong et al., 2007), the lowest correlation coefficient (r) found was in the study of Briggs (2007) (Briggs et al., 2007). In this study, the authors correlated the T1--T12 Cobb with T1-T12 Centroid (r = 0.84) in a sample of women with osteoporosis, identifying poor correlation between Cobb and Centroid of 58,25º in greater kyphosis, because the Cobb is affected by plateaus terminals of the vertebrae, which may have fractures, resulting in higher angulation. In contrast, the highest value of correlation found was in the study of Goh (2000) (Goh et al., 2000), which the r was 0.98, which correlated the results of Cobb T4 to T9 to alternative Cobb T4, arguing that the latter method seems to be more recommended for being simpler and does not take into account the deformation of the vertebral plateaus in their formation. Goh (2000) (Goh et al., 2000) concluded in his study that, due to the simplicity of the method and ease in in viewing plateaus, alternative Cobb T4-T9, or even the Radius of curvature T4, T9 should be used to evaluate the thoracic curvature of individuals with normal or increased kyphosis, since it has no good correlation with Cobb in subjects with kyphosis lower than 20º.
Each study sustains and discusses the use of certain methods according to their findings, which often contradict each other, but all corroborate in order to find the best method for evaluating lumbar lordosis. Harrison (2001) (Harrison, Harrison, et al., 2001) defends that the method of posterior Tangents and the Centroid are more recommended in the analysis of lumbar curvature for not using a potential source of error as the vertebral plateaus. Troyanovich (1998) (Troyanovich et al., 1998) supports the use of the posterior Tangents to be less susceptible to errors like those found in the Cobb, besides presenting lower SEM and acceptable ICCs.
Chanplakorn (2011) (Chanplakorn et al., 2011) and Gardocki (2002) (Gardocki et al., 2002) believe that lumbar lordosis is directly influenced by the magnitude degree of pelvic tilt, because they take into account the trunk imbalances, and therefore, the analysis of this segment is inevitable. They concluded that the PR measure can be useful to evaluate functional results of a spinal fusion in patients with sagittal imbalance. Jackson (1998) (Jackson et al., 1998a) reaffirms this importance when reports using the PR for evaluating lumbar lordosis, since it takes the sacrum and pelvis into consideration. The author describes these segments act as a sixth lumbar or pelvic vertebra to define a column arc. Jackson (2000) (Jackson et al., 2000b) states that the PR technique is more recommended to quantify the lumbar lordosis because it has good reproducibility, and can determine the sagittal pelvic imbalance through the hip.
Also, even more important, because the PR and Cobb measures correlate and complement each other to settle lumbar lordosis.
When analyzing the reliability of an evaluation method, it is important to identify the mean absolute diffe-rence (MAD) of observers measures, which are determined to provide an error analysis, in that the higher the MAD values are, the greater the variability measure is.
The MAD inter-rater values verified in Lee's work (2013) (Lee et al., 2013b) were: centroid L1-L5 (7,1º), TRALLL1-S1 (6.4°) and posterior Tangent L1-S1 (5,7º), all higher than the values found in the gold standard, Cobb L1-L5 (3,4º) and Cobb L1-S1 (4,4º). The author explains that all values were considered high, and attributes this to the fact that many people in the sample were suffering from ankylosing spondylitis, resulting in many irregularities in the vertebrae. In contrast, Chen (1999) (Chen, 1999) reports that the centroid method MAD has lower values and higher ICCs rates in comparison to Cobb, in healthy persons, and because of this, is more reproducible and recommended than the previous. Chernucka (1998) (Chernukha et al., 1998)  Regarding the evaluation of the lumbar spine in specific populations, individuals with severe scoliosis ob- Chernucka (1998) (Chernukha et al., 1998) describes that the quality and the degree of distortion of the radiographic image and wedge-shaped plateaus, features found in people with osteoporosis, osteomalacia, skeletal imaturation, disc herniation or espondiloarthrosis are factors that influence the Cobb angular formation and may overestimate or underestimate the angle of curvature. Therefore, the authors believe that the TRALL is more advantageous because it does not depend on the plateaus and has better reproducibility than the Cobb in the evaluation of the lumbar spine of children and adolescents (Chernukha et al., 1998).
Few studies that showed concurrent validity data lumbar lordosis between the proposed new method and Cobb (Gardocki et al., 2002;Mac-Thiong et al., 2007;Vacari et al., 2015). Pinel- Despite the not constricted Cobb technique take longer than Cobb, it shows better reproducibility rates, and the great advantage of this method is to take into account the variability in the level of transition between kyphosis and lordosis, allowing better assessment of the magnitude of curvatura (Mac-Thiong et al., 2007).
The author found good correlation between Cobb L1-S1 methods with not constricted Cobb, demonstrated by an r = 0.94. This method is concerned with the variation in the transition between the curvature of kyphosis and lordosis (Mac-Thiong et al., 2007), and that the column disorders treatments can affect the length of the back, for example, in spondylolisthesis. Gardocki (2002) (Gardocki et al., 2002) correlated their method, the PR-L1 with Cobb L1-S1 and found an r = 0.82 (0 <0.001). The authors support the use of PR--L1, because it takes into account the lumbo-pelvic segment that can undergo modifications due to a poor sagittal balance, changing the lumbar lordosis. This finding is especially important in assessing patients with problems in this compensation, which are limited in some surgical procedures such as lumbar fusion, indicated in patients with flexion contracture of the hip or arthritis at this location, and depending on the degree of change, an analysis cautious about it, should be considered. Despite the lack of studies investigating these situations and relationships, they anticipate that the PR technique will be widely used in prediction of patient satisfaction and functional results after lumbar fusion and evaluation of patients with sagittal imbalance. It is worth noting that most studies examined the adult population. Children, adolescents and the elderly who tend to have vertebral deformities were studied in only six of all studies found. The adults analyzed were not always healthy, therefore, also showing deformation or some difficulty in analyzing the vertebral levels to be assessed in many cases.

CONCLUSION
Of the 23 studies included in this review, only two did not present high methodological quality (Rajnics et al., 2001;Hicks et al., 2006). As for the reproducibility and repeatability, the Centroid, posterior Tangent and TRALL methods demonstrated equal or better reproducibility values and less variability of measures when compared to the Cobb angle. However, it is suggested that its use is confined to clinical monitoring, since they have no information on their validation, not being suitable for diagnostic measurements.
As to concurrent validity alternative methods: (1) in the thoracic region (Centroid T1-T12, tangential circles, alternative Cobb T4-T9, Radius of curvature, and not constricted Cobb) and (2) in the lumbar (PR-L1, tangential circles and not constricted Cobb) showed strong correlation with the gold standard (Cobb T1--T12). These results suggest that these methods are accurate and reliable for the evaluation of sagittal spinal column.