How Does the Slump Sitting Radiograph Increase Proportion of Segmental Instability and Kyphotic Alignment of Lumbar Degenerative Spondylolisthesis?

Abstract

Objective

Clinical and radiographic degenerative spondylolisthesis (CARDS) classification was proposed to differentiate homogenous lumbar degenerative spondylolisthesis (LDS) subgroups. The sitting radiograph exhibited lumbar malalignment with maximum lumbar kyphosis, intervertebral kyphosis, and spondylolisthesis.This study aimed to assess the sitting radiograph for distribution of clinical and radiographic degenerative spondylolisthesis classification, and to elucidate its significance for exhibiting kyphotic alignment (CARDS type D) and segmental instability.

Methods

A cohort of 101 patients with symptomatic lumbar degenerative spondylolisthesis (LDS) between September 2018 and December 2020 were recruited. The distribution and relibility of CARDS classification with or without sitting radiograph was assessed. The translational and angular range of motion and segmental instability was also evaluated. Univariate analysis of variance was used for multiple groups, and the least significant difference for two groups. Kappa consistency test of intrarater and interrater was evaluated for CARDS classification with or without sitting radiograph. Chi‐square test was used to compare paried categorical data.

Results

Utility of sitting radiographs for CARDS classification revealed higher percentage of type D than that without the sitting radiograph (p < 0.001). The sitting radiograph revealed a larger slip distance than the flexion radiograph (p = 0.003), as well as a lower slip angle than flexion radiograph (p < 0.001). The sitting‐supine modality demonstrated the largest translational range of motion compared to the sitting‐extension (p < 0.001) and flexion‐extension modalities (p < 0.001). The sitting‐supine modality showed larger angular range of motion than the flexion‐extension modality (p < 0.001). The percentage of flexion, extension, upright, supine, and sitting radiograph to identify translational instability was higher than that without sitting radiograph (p < 0.001), as well as taking angular motion ≥10° as an additional criterion for segmental instability (p < 0.001).

Conclusion

The CARDS classification was reliable for LDS. The sitting radiograph showed maximal slip distance and kyphotic slip angle. Application of the sitting radiograph was necessary for evaluating segmental instability and kyphotic alignment of LDS.

Clinical and radiographic degenerative spondylolisthesis (CARDS) classification was proposed to differentiate homogenous lumbar degenerative spondylolisthesis (LDS) subgroups (A). A patient diagnosed with L4/5 LDS received sitting (B), standing upright (C), standing flexion (D), standing extension (E), and supine CT images (F). According to the standing upright, flexion, extension, and the supine CT image, the patient was characterized with CARDS type B. However, the patient was distributed to CARDS type D in reference to the kyphotic alignment on sitting radiograph.

Introduction

Lumbar degenerative spondylolisthesis (LDS) is becoming more common as society ages. ¹ , ² , ³ , ⁴ At the same time, LDS‐related symptoms usually get worse with aging. ² If conservative treatment does not work, surgical treatment is considered for patients with severe symptoms. ² There is a tendency towards fusion surgery for diagnosis of segmental instability; however, LDS is a heterogeneous disease with wide variation in disk collapse, sagittal malalignment, translational motion, as well as segmental instability. ¹ , ² , ³ , ⁴ , ⁵ , ⁶ , ⁷ , ⁸ , ⁹

Clinical and radiographic degenerative spondylolisthesis (CARDS) classification was recently proposed to differentiate homogenous LDS subgroups. ¹⁰ , ¹¹ This classification is based on heterogeneous radiographic variations in disk height, lumbar alignment, vertebral translation, and lower extremity symptoms. ¹⁰ , ¹¹ This scheme facilitates communications to enhance the quality of outcomes research on LDS. It has been validated for its reliability; however, only a small cohort of patients with neutral, flexion, and extension lateral radiographs were applicable for development and reliability of this classification. ¹⁰ , ¹¹ Nevertheless, the flexion‐extension radiological assessment of LDS is challenged for reasons of external radiation and unbearable for compulsory experimental postures. ¹ , ² , ³ , ⁴ , ⁵ , ¹² Some studies reported lumbar sagittal malalignment in different postures, particularly in the sitting radiograph. ¹ , ¹² , ¹³ The sitting radiograph exhibited lumbar malalignment with maximum lumbar kyphosis, intervertebral kyphosis, and spondylolisthesis. These features were necessary for making diagnosis and developing treatment algorithm. ¹ , ¹² , ¹³ However, the sitting radiograph was not taken into considerations in CARDS classification. ¹ , ¹⁰ , ¹¹ , ¹² Whether the sitting radiograph influences the distribution of CARDS classification is not clear.

Evaluation of segmental instability in LDS is also a classic topic in spite of no consistency for the standard criteria of segmental instability. ¹ , ² , ³ , ⁴ , ⁵ , ⁶ , ¹² , ¹⁴ , ¹⁵ Assessment of segmental instability should be explored in combination with the sitting radiograph, which may be added to the radiographic variables for CARDS type D. Previous studies of sitting radiograph drew limited conclusions of sitting radiograph in measuring angular range of motion or in the measurement of displacement. ¹ , ¹⁶ It is necessary to evaluate the sitting radiograph with a large cohort of LDS patients.

This study was undertaken to: (i) monitor the reliability and distribution of CARDS classification through standing flexion, upright, extension, supine, and sitting radiographs; (ii) to exhibit the extreme lumbar malalignment morphology by comparing the range of motion of LDS patients between radiographs.

Methods

Patients

We retrospectively recruited patients with symptomatic LDS between September 2018 and December 2020. A consecutive cohort of surgical patients due to them having L4/5 low‐grade (Meyerding I or II) degenerative spondylolisthesis were enrolled in this study. The vertebral arch was intact on 3D‐CT radiographs of the lumbar spine. Patients were excluded if they had lumbar scoliosis >10°, history of spine, pelvic or hip joint fracture, or surgery. Eventually, a cohort of 101 patients with demographic data were enrolled.

Radiographic Assessment

Each patient received a set of standing flexion, standing upright, standing extension, supine CT images, and slump sitting radiograph. The standard procedure of radiography was described by the previous study. ¹ , ⁴ Slip distance and slip angle was measured as per previous description. ¹ , ⁴ Range of motion between different postures was calculated, including intervertebral translational motion and angular rotation. Translational range of motion ≥4 mm was identified with segmental instability, and angular range of motion ≥10° acted as a catalyst to reinforce identification of segmental instability. ¹ , ² , ⁴ , ⁵ , ¹²

CARDS Classification System

As was defined by Kepler et al., ¹⁰ we described the flow diagram of classic CARDS classification based on the neutral, flexion, and extension lateral radiographs  (Figure 1). In a nutshell, patients with kyphotic alignment on any lateral views were defined as type D, and loss of disc were defined as type A. Others with translation less than 5 mm or not were sub‐grouped into type B or C. Furthermore, absent, unilateral, or bilateral leg pain during the medical history was designated with the modifier 0, 1, 2, respectively. Additionally, the sitting radiograph and supine image of patient was applied to classify CARDS scheme in this study (Figure 2). Radiographs of patients were retrospected by five reviewers to determine CARDS types.

FIGURE 1.

Flow diagram of classical clinical and radiographic degenerative spondylolisthesis (CARDS) classification.

FIGURE 2.

A patient diagnosed of L4/5 lumbar degenerative spondylolisthesis (LDS) received sitting (A), standing upright (B), standing flexion (C), standing extension (D), and supine CT images (E). According to the standing upright, flexion, extension, and the supine CT image, the patient was characterized with classical clinical and radiographic degenerative spondylolisthesis (CARDS) type B. However, the patient was distrbuted to CARDS type D in reference to the kyphotic alignment on sitting radiograph.

Intra‐ and Interrater Reliability Study

Kappa consistency test, also known as Cohen's Kappa, was analyzed for intrarater reliability. Fleiss’ kappa coefficient was analyzed for interrater reliability. With reference to Kepler et al., ¹⁰ the first grading of all observers was compared for interobserver reliability. Kappa values were analyzed as follows: less than 0 for no agreement, 0–0.20 for slight, 0.21–0.40 for fair, 0.41–0.60 for moderate, 0.61–0.80 for substantial, and 0.81–1.0 for near‐perfect, respectively.

Statistical Analysis

Radiographic parameters were measured three times by Surgimap Spine software (version: 2.2.12.1, Nemaris, USA). SPSS version 20.0 was used for statistical analysis. GraphPad Prism (version 9.0 GraphPad Software, San Diego, California, USA) was used to draw the histogram. The average slip distance and slip angle of the three measurements was included in this study. Univariate analysis of variance (ANOVA) was used for multiple groups, and the least significant difference (LSD) for two groups.

First, Kappa consistency test of intrarater and interrater was evaluated for CARDS classification with or without sitting radiograph. Second, the distribution of CARDS classification was compared with or without sitting radiograph. Third, the measurements of different radiographs were compared to exhibit the suitable slip distance and slip angle by univariate ANOVA and LSD for evaluating range of motion. Forth, the differences of translational and angular range of motion were compared by univariate ANOVA and LSD for evaluation abnormal intervertebral movement. Finally, the χ ²‐test was used to compare the proportion of segmental instability between the scheme proposed in this study and the traditional flexion‐extension method. p < 0.05 indicated statistical differences.

Results

CARDS Classification Reliability and Distribution

The intrarater reliability analysis for classic CARDS classification without sitting radiograph demonstrated κ‐values of 0.86 for all patients. The interrater reliability analysis demonstrated κ‐values of 0.82 for all patients. Taking sitting radiograph for analysis, the κ‐values were 0.84 for the intrarater reliability, and 0.80 for the interrater reliability.

The distribution of CARDS classification without sitting radiograph were 3.0% for Type A, 36.6% for Type B, 39.6% for Type C, and 30.7% for Type D, respectively. With sitting radiograph taken into consideration, the distribution was 3.0% for Type A, 5.9% for Type B, 28.7% for Type C, and 62.4% for Type D, respectively. There were statistical differences of the distribution of CARDS classification with or without sitting radiograph (p < 0.001) (Table 1). The flexion, extension, upright, supine with addition of sitting radiograph for CARDS classification revealed higher proportion of type D than that without sitting radiograph (32/101 vs. 60/101, p < 0.001).

TABLE 1.

Distribution of CARDS classification with or without sitting radiograph.

Sitting, flexion, extension, upright	Flexion, extension, upright				Total
	A	B	C	D
A	3	0	0	0	3
B	0	6	0	0	6
C	0	9	20	0	29
D	0	12	20	31	63
Total	3	37	40	31	101

Abbreviation: CARDS, classical clinical and radiographic degenerative spondylolisthesis.

Intervertebral Translational and Angular Range of Motion

Univariate ANOVA demonstrated statistical differences of slip distance among flexion, extension, upright, supine, and sitting radiographs (p < 0.001) (Figures 2 and 3). The sitting radiograph revealed a larger slip distance than the standing upright (p = 0.003) or standing flexion radiograph (p = 0.003). The supine sagittal CT and the standing extension radiograph exhibited similar slip distance (p = 0.192). Similarly, there were statistical differences of slip angle among flexion, extension, upright, supine, and sitting radiographs (p < 0.001). The sitting radiograph had a lower slip angle than the standing flexion radiograph (p < 0.001).

FIGURE 3.

Slip distance and slip angle in the five postures radiographies. Univariate ANOVA demonstrated statistical differences of slip distance (p < 0.001) (A) and slip angle (p < 0.001) (B) among flexion, extension, upright, supine, and sitting radiographs. The sitting radiograph revealed the larger slip distance than the standing upright (p = 0.003) or flexion radiograph (p = 0.003). The supine sagittal CT and the standing extension radiograph exhibited similar slip distance (p = 0.192). The sitting radiograph had a lower slip angle than standing flexion radiograph (p < 0.001).

Based on the statistical differences of translational range of motion (p < 0.001), the sitting‐supine modality demonstrated the largest translational range of motion than the sitting‐extension (p < 0.001) and flexion‐extension modalities (p < 0.001) (Figures 2 and 4). The flexion‐extension modality showed lower angular range of motion than the sitting‐supine modality (p < 0.001) and the sitting‐extension modality (p < 0.001).

FIGURE 4.

Translational and angular range of motion. Based on the statistical differences of translational range of motion (p < 0.001), the sitting‐supine modality demonstrated the larger translational range of motion than the sitting‐extension (p < 0.001) and flexion‐extension modalities (p < 0.001). The flexion‐extension showed lower angular range of motion than the sitting‐supine modality (p < 0.001) and the sitting‐extension modality (p < 0.001).

Comparison of the Diagnostic Algorithms with or without Sitting Radiograph

We demonstrated that the ability of flexion, extension, upright, supine and sitting radiograph to identify translational instability was higher than that without the sitting radiograph (28/101 vs. 56/101, p < 0.001) (Table 2). Moreover, taking angular motion ≥10° as an additional criterion for segmental instability, the modality with the sitting radiograph also demonstrated larger percentage of segmental instability than that without sitting radiograph (8/101 vs. 31/101, p < 0.001) (Table 3).

TABLE 2.

Comparison of percentage of patients with diagnosis of single translational instability made by dynamic radiographs with or without sitting radiograph.

Sitting, flexion, extension, upright, supine	Flexion, extension, upright, supine		Total
	Translational motion ≥4 mm (translational instability)	Translational motion <4 mm
Translational motion ≥4 mm (translational instability)	28	28	56
Translational motion <4 mm	0	45	45
Total	28	73	101

TABLE 3.

Comparison of percentage of patients with angular motion ≥10° and translational instability made by dynamic radiographs with or without sitting radiograph.

Sitting, flexion, extension, upright, supine	Flexion, extension, upright supine		Total
	Segmental instability (translational motion ≥4 mm and angular motion ≥10°)	Segmental stability
Segmental instability (translational motion ≥4 mm and angular motion ≥10°)	8	23	31
Segmental stability	0	70	70
Total	8	93	101

Discussion

This study demonstrated near‐perfect intra‐ and interrater reliablity of CARDS classification on the basis of its classic criteria. CARDS classification plans to reproducibly categorize subgroups of LDS patients based on radiographic and clinical features. ¹⁰ , ¹¹ Besides external validation, this classification is high intra‐ and interrater reliable, indicating that it is useful in defining radiographic subgroups of LDS patients when conducting clinical research. Nevertheless, the classification is only based on the flexion, extension, upright, and supine radiographs. As a physical position, the sitting radiograph for clinical diagnosis and evaluation of LDS is causing wide concerns. ⁴ , ¹² , ¹³ Lumbar kyphotic alignment in the sitting radiograph exhibits large spondylolisthesis. Nevertheless, these surprising findings have not been applied to classify this heterogeneous disease. Increased proportion of type D was attributed to the application of the sitting radiography. Utility of the sitting radiograph showed larger translational and angular motion, which was superior to other radiographs in revealing extreme status of lumbar malalignment.

The Necessity the Slump Sitting Radiograph of CARDS Classification for LDS

Our study demonstrated near‐perfect intra‐ and interrater reliablity of CARDS classification on the basis of its classification criteria with or without sitting radiograph.The current literature on LDS treatments almost exclusively lumped all patients together, making it impossible to understand the makeup of a particular study population and compare patients between studies. ² In view of the urgency of this confusion, CARDS classification were proposed to reproducibly categorize subgroups of LDS patients. ¹⁰ There was a study that reported reliability of the CARDS classification; however, they did not improve the application of the classification due to its small sample size. ¹¹ Here, we spared no effort to deepen the reformation of the CARDS classification for the treatment strategy and clinical guideline.

The current study found that the sitting radiograph changed the distribution of CARDS classification. As was revealed by distribution of CARDS classification with or without sitting radiograph (Table 1), utility of the sitting radiograph statistically enhanced the ratio of type D with reduced type B and type C. Actually, the percentage of type D without sitting radiograph in our study was higher than that in the proposer of CARDS classification and its reliability study. ¹⁰ , ¹¹ This bias was probably attributed to the fact that the enrolled patients were all received surgical treatment. This also indicated the importance of type D for LDS patients. Nevertheless, sitting radiograph further exaggerated the ratio of type D. These data were accessible due to the kyphotic alignment of lumbar spine in sitting radiograph. ¹ , ¹² , ¹³ To some extent, the sitting radiograph further differentiated subgroups of LDS and led to a new understanding of LDS. ¹ , ¹² , ¹³ This phenomenon attributed to the lumbar kyphosis, intervertebral kyphosis, and amplified anteriolisthesis in sitting radiograph. We expected more and high‐quality research to elucidate the sitting radiograph and the classification for precision medicine.

The Importance of Evaluating Vertebral Stability

The CARDS classification facilitates communication between clinicians and promotes high‐quality outcomes research up to a point. Nevertheless, many studies and experts point out that the evaluation of segmental instability contributes directly to the surgical strategy. ¹ , ² , ⁴ It is here that various researchers' different studies converge: the evaluation of segmental instability was significant for lumbar surgical strategy, including decompression, decompression with fusion, or interbody fusion. ¹ , ² , ³ , ⁴ , ⁵

The criteria and definition of segmental instability are still controversial; however, the radiogrophic evaluation acted as a catalyst for the diffused points to converge. ¹ , ² , ³ , ⁴ , ⁵ The clinical symptoms derived from patient daily dynamic activity. Therefore, the range of motion between two postures for segmental instability was more reasonable than single posture. ¹ , ² , ³ , ⁴ , ⁵ For the past decades, the standard criteria for interbody range of motion was the standing flexion with extension radiograph. Some studies have sprung up to challenge this modality. ¹ , ² , ³ , ⁴ , ⁵ , ⁷ , ¹² , ¹⁷ The flexion and extension was forced postures, particularly for patients with back pain and neurologic symptoms. It was worth mentioning that sitting radiograph can exhibit maximal anterolisthesis and kyphotic interverbebral angle of LDS. In this regard, the sitting radiograph should be added to the assessment of the segmental instability of LDS. Advantages of utilized sitting radiograph will be discussed later.

Utility of the Sitting Radiograph for Assessment of the Lumbar Spine

This study demonstrated that the sitting radiograph revealed the maximal anteriolisthesis based on a large cohort of LDS patients in a single center. Furthermore, this study demonstrated that the sitting radiograph exhibited an average kyphotic alignment of LDS, which was also known as CARDS type D. Utility of sitting radiograph revealed greater translational and angular range of motion of segmental instability, corresponding with larger ratio of CARDS type D. This correlationship further emphasized that the sitting radiograph was significant for evaluating LDS. A previous study reported the superiority of slump sitting radiograph in assessing angular range of motion not but in the displacement. ¹² This inconsistency may be attributed to the enrolled participants, who were recruited from the specialist outpatient clinic. ¹² These patients may not be diagnosed with spondylolisthesis, which explained no statistical differences of translational range of motion between sitting and flexion ragiographs. ¹² Recently, a study described a similar conclusion of sitting radiograph in the measurement of vertebrae displacement. ¹ However, they only demonstrated the superiority of sitting radiogrpah for anteriolisthesis. Their study did not conclude statistical differences for intervertebral angle between sitting and flexion due to a limited cohort. ¹

Sagittal malalignment contributes directly to patients’ reported outcomes after lumbar fusion and adjacent segment diseases. ¹ , ⁶ , ¹⁰ Postoperative lumbar lordosis was reported to associate with patient‐reported outcomes of LDS. ⁶ , ¹⁶ , ¹⁸ , ¹⁹ The kyphotic alignment (CARDS type D) were possibly characterized with insufficient anterior column support and inadequate motion of the functional spinal unit. ¹ , ¹⁰ , ¹⁴ , ¹⁵ , ²⁰ Generally, posterior instrumentation and additional interbody fusion was recommended for CARDS type D. However, a high ratio of kyphotic alignment in combination of sitting radiograph may result in excessive fusion surgery. We proposed patients with kyphotic alignment and segmenal instability as a unique subgroup, along with recommendation with additional fusion surgery. We expect that high‐quality randomized controlled trials are needed to elucidate the sitting radiograph for the diagnosis and treatment algorithms for LDS.

Strengths and Limitations

Notably, the sitting radiograph shows maximal slip distance and kyphotic slip angle.The sitting‐supine modality demonstrates the large translational range of motion and angular range of motion, and segmental instability. Patients with kyphotic alignment (CARDS type D) and segmental instability seem to be a special subgroup. Application of the sitting radiograph is necessary and significant for establishment treatment algorithms of LDS.

This study has several limitations. This retrospective study enrolled a case series of patients who were expected to be operated on. The enrolled preoperative patients may represent a quite serious disease condition. Nevertheless, this classic representation greatly attracted surgeons’ attention. The findings of sitting radiograph in this study can thoroughly manifest its significance due to those biases. Second, the radiographs were not conducted randomly; however, patients were forced to rest for more than 10 min before each examination to decrease the bias. Third, the segmental instability criteria were still disputable. The core of this study was to emphasize the special significance of sitting radiograph for highlighting the heterogeneity of LDS.

Conclusion

The CARDS classification is reliable for evaluation of LDS. The sitting radiograph exhibits significant anteriolisthesis and slip angle. The sitting radiograph for CARDS classification reveals high percentage of type D kyphotic alignment. The sitting‐supine modality demonstrates the large translational range of motion and angular range of motion, and segmental instability. Application of the sitting radiograph is necessary and significant for establishing treatment algorithms of LDS.

Author Contributions

Conceptualization: Xu Sun, Yong Qiu. Methodology: Qingshuang Zhou, Xu Sun, Bin Wang. Investigation: Qingshuang Zhou, Xu Sun, Zezhang Zhu. Formal Analysis: Qingshuang Zhou, Xu Sun. Resources: Xu Sun, Bin Wang, Zezhang Zhu, Yong Qiu.Writing—Original Draft: Qingshuang Zhou.Writing—Review and Editing: Xu Sun, Yong Qiu.Visualization: Bin Wang, Zezhang Zhu. Supervision: Xu Sun, Yong Qiu. Funding Acquisition: Qingshuang Zhou, Xu Sun, Yong Qiu.

Funding Information

Qingshuang Zhou has received funding from Postgraduate Research & Practice Innovation Program of Jiangsu Province (No. KYCX22_3709), Xu Sun has received funding from the National Natural Science Foundation of China (No. 81772422), and Yong Qiu has received funding from Jiangsu Provincial Key Medical Center (No. YXZXA2016009).

Conflict of Interest Statement

The authors declare no conflicts of interests.

Ethics Statement

This study was approved by the Ethics Committee (2021‐398‐01, 2020‐028‐01).