
==== Front
J Orthop Surg Res
J Orthop Surg Res
Journal of Orthopaedic Surgery and Research
1749-799X
BioMed Central London

39223662
5033
10.1186/s13018-024-05033-y
Research Article
Segmental vertebral three-dimensional motion in patients with L4 isthmic spondylolisthesis under weight-bearing conditions
Xu Hongda
Deng Haitao
Li Mingfan
Wang Tieheng
Qing Peidong qingpeidong@163.com

Spinal Surgery Department of Mianyang Orthopedic Hospital, No. 158, Changhong Avenue South Section, Fucheng District, Mianyang, 621000 Sichuan Province China
2 9 2024
2 9 2024
2024
19 5348 4 2024
27 8 2024
© The Author(s) 2024
2024
https://creativecommons.org/licenses/by-nc-nd/4.0/ Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
Objective

To investigate in vivo 6-degree-of-freedom (DOF) vertebral motion in patients with isthmic spondylolisthesis (IS) during various functional weight-bearing activities.

Methods

Fifteen asymptomatic volunteers (mean age 54.8 years) and fourteen patients with IS at L4-5 (mean age 53.4 years) were recruited. The positions of the vertebrae (L4-L5) in the supine, standing, flexion–extension, left–right twisting and left–right bending positions were determined using previously described CT-based models and dual fluoroscopic imaging techniques. Local coordinate systems were established at the center of the anterior vertebra of L4 isthmic spondylolisthesis (AIS), the posterior lamina of L4 isthmic spondylolisthesis (PIS) and the center of the L5 vertebra to obtain the 6DOF range of motion (ROM) at L4-L5 and the range of motion (ROM) between the AIS and the PIS.

Results

The translation along the anteroposterior axis at L4-L5 during flexion–extension, left–right bending and left–right twisting was significantly greater than that of the healthy participants. However, the translation along the mediolateral axis at L4-L5 presented paradoxical motion under different positions: the ROM increased in the supine-standing and flexion–extension positions but decreased in the left–right bending and left–right twisting positions. The separation along the anteroposterior axis during flexion was significantly greater than that during standing, on average, reaching more than 1 mm. The separation along the mediolateral axis during standing, flexion and extension was significantly greater than that in the supine position.

Conclusions

This study revealed the occurrence of displacement between the AIS and PIS, primarily in the form of separation during flexion. Symptomatic patients with isthmic spondylolisthesis exhibit intervertebral instability, which might be underestimated by flexion–extension radiographs.

Keywords

Lumbar spine motion
Lumbar isthmic spondylolisthesis
In vivo kinematics
Fluoroscopy imaging
Functional weight-bearing activities
The China National Natural Science Foundation81371992 issue-copyright-statement© BioMed Central Ltd., part of Springer Nature 2024
==== Body
pmcIntroduction

Isthmic spondylolisthesis (IS) is defined as the slip of a vertebra in relation to an adjacent vertebra due to a defect in the pars interarticularis, also known as spondylolysis, with a prevalence of 3%-10% in the general population. An IS is a complication of spondylolysis resulting from a loss of posterior stabilization in the affected segment [1, 2]. In contrast to degenerative spondylolisthesis, axial low back pain is the most common symptom of IS [3]. Forward slip of the vertebral body itself does not typically result in foraminal or central stenosis, and complete occlusion of the cauda equina is unlikely [4]. Therefore, quantitative knowledge of intervertebral motion at diseased segments under physiological weight-bearing conditions is instrumental for obtaining a better understanding of the biomechanical factors associated with the IS and improving surgical treatment efficacy [5].

The kinematics of the lumbar spine have been studied with the use of a variety of techniques, including flexion–extension radiographs, biplanar radiographs, traction-compression radiographs, stereophotogrammetric methods, and open MRI [6–11]. However, most of these studies focused on motion in select planes under nonphysiological loading conditions or presented conflicting results [12, 13]. Although positional-upright MR, which combines the benefits of conventional MRI and functional radiography, is thought to be the most sophisticated imaging tool for assessing IS, dynamic imaging with an open MR device has several drawbacks. These include the reduced signal/noise ratio due to the lower field strength, the limited postures that the patient may hold without moving or experiencing pain, and possible underestimation of the extent of disease in the seated position compared with the standing position [14, 15]. Therefore, the in vivo 3D motion characteristics of IS are not well understood. In addition, there may be small motions between the vertebral body and the posterior elements that have not been confirmed in the literature due to technical difficulty.

Recently, we utilized a combined dual fluoroscopic and MRI/CT imaging system (DFIS) to investigate in vivo lumbar spine kinematics in human subjects [16–20]. We studied a cohort of patients with IS immediately prior to spinal surgery and compared the results with those of an asymptomatic group without evidence of lower back pain or other spinal disorders. We hypothesized that symptomatic lumbar vertebrae at the slipped level would demonstrate distinct motion patterns during active in vivo spine motion prior to spinal surgery.

Methods

Subjects

Approval of the experimental design by the authors’ Institutional Review Board was obtained prior to the initiation of the study. Informed consent was obtained from each subject before any testing was performed. Fourteen symptomatic patients with a diagnosis of L4–5 IS (seven men and seven women) were recruited from a single academic center. The patients had a mean age of 53.4 years (ranging from 46 to 61 years), a mean height of 173.3 cm, and a mean weight of 70.8 kg. Inclusion criteria: A clear diagnosis of L4 IS was identified by medical history, symptoms and imaging studies and all were bilateral spondylolysis. The exclusion criteria included previous spinal surgery, degenerative spondylolisthesis, trauma, scoliosis, L4-5 disc herniation without isthmic spondylolisthesis, tumors, paralysis, spinal cord disease, psychiatric histories, radiation treatment within the previous year, and pregnancy. The chief complaint for all patients was mechanical low back pain, worsened during standing or walking but might be relieved in the supine or flexed position, which was consistent with lumbar instability, but flexion–extension radiographs might have no obvious abnormalities; all patients underwent conservative treatment for a minimum of six months without experiencing significant improvement. Two patients had varying levels of radicular pain radiating into the buttocks and posterior thighs. Radiographic confirmation of low back pain originating from the L4-5 IS was determined by the treating surgeon and a neuroradiologist. Seven patients had grade I vertebral slippage, and the others had grade II vertebral slippage according to the Meyerding classification method [21].

Fifteen asymptomatic subjects (nine men and six women) ranging from 50 to 63 years of age were recruited (mean age, 54.8 years; mean height, 170.8 cm; mean weight, 66.1 kg). The subjects were evaluated for the absence of spondylolisis or spondylolisthesis as well as lack of evidence of low back pain (past or present) and other spinal disorders. The data from this group of normal subjects served as a control (Table 1).Table 1 General condition of both groups(Mean ± SD)

	N	Age(Y)	Gender	Height(M)	Weight(Kg)	
Male Female	
IS	14	53.43 ± 8.52	7 7	1.73 ± 0.03	70.86 ± 5.08	
Nomal	15	54.80 ± 9.28	9 6	1.70 ± 0.08	66.10 ± 11.14	
The symbols(*)represent statistical significance on between-group comparison (P < 0.05)

Three-dimensional CT-based model

All subjects were scanned in the supine relaxed position in a General Electric Light Speed Pro16 CT scanner (Siemens 16, Siemens, Germany). Parallel digital images with a thickness of 0.75 mm and a resolution of 512 × 512 pixels were obtained. The CT images of the spinal segments were then imported into modeling software (Rhinoceros; Robert McNeel & Associates, Seattle, Washington) to construct 3D anatomical vertebral models of the lumbar spine [16, 20]. The contours of the vertebrae were manually digitized with the use of B-spline curves. Mesh models of the vertebrae were then created from the contours (Fig. 1). The mean accuracy of our image-matching technique in determining translation has been shown to be 0.35 mm. The repeatability of the method in reproducing in vivo human spine six-degree-of-freedom kinematics was < 0.4 mm in translation and < 0.6° in orientation [16].Fig. 1 A, Digitized contours of lumbar vertebrae of patients with IS at L4-L5 in the sagittal plane. B, Three-dimensional anatomic vertebral model of L3–S1, constructed from CT images. IS indicates isthmic spondylolisthesis

Dual fluoroscopic imaging

The lumbar spines of the subjects were imaged with the use of a dual orthogonal fluoroscopic system (Toshiba SXT-1000A, Japan) (Fig. 2A) [16]. The subjects were asked to stand and position their lumbar spines within the field of view of both fluoroscopes and actively move to different postures: standing upright, 45° flexion of the trunk relative to the vertical, maximal extension, maximal left–right bending, and maximal left–right torsion. For each selected posture, the participant was asked to hold still for approximately 1 s while the two fluoroscopes took simultaneous images from two orthogonal directions. The postures were carefully monitored by an orthopedic surgeon to reduce variation. A special pelvic limiter was applied to the hips of the participants to minimize their hip motions while they performed active motions to maximize lumbar spine motion and to position the lumbar spine within the field of view of the two fluoroscopes. Images were taken as described in a previous paper [16, 20].Fig. 2 A, Dual fluoroscopic imaging system (DFIS) setup for imaging the lumbar spine in vivo consists of two fluoroscopes positioned in two orthogonal planes. A special pelvic limiter was applied to the hips of the participants to minimize their hip motions while they performed active motions, in order to maximize lumbar spine motion and to position the lumbar spine within the field of view of the two fluoroscopes. B, virtual reproduction of the in-vivo position of the lumbar vertebrae in modeling software

Reproduction of lumbar spine kinematics under in vivo weight bearing

The pair of fluoroscopic images captured at a specific posture was imported into the modeling software and placed in calibrated orthogonal planes, reproducing the positions of the intensifiers. Two virtual cameras were created inside the virtual space to reproduce the positions of the X-ray sources with respect to the image intensifiers. Thus, the geometry of the dual-orthogonal fluoroscopic system was recreated. The vertebral models were introduced into the virtual system and were viewed from the perspective of the two virtual cameras (Fig. 2B). The models were independently translated and rotated in six degrees of freedom (that is, the set of independent displacements and/or rotations that specify completely the displaced position and orientation of a rigid body) until their outlines matched those captured on the two orthogonal fluoroscopic images according to an existing protocol established in our laboratory [16, 17, 19, 20, 22]. The software allowed the model to be manually translated and rotated in increments of 0.01 mm and 0.01°, respectively. The vertebral positions during in vivo weight-bearing activities were reproduced, representing the six-degree-of-freedom kinematics of the vertebrae at each in vivo posture.

Measurements of variables

We divided the L4 vertebra into two segments. The anterior segment of isthmic spondylolisthesis (AIS) consists of the vertebral body with the pedicles, transverse processes, and superior articular processes; the posterior segment of isthmic spondylolisthesis (PIS) consists of the inferior articular processes, laminae, and spinous process (Fig. 3). Right-hand Cartesian coordinate systems were established at the center of the anterior vertebra of L4 isthmic spondylolisthesis (AIS), the posterior lamina of L4 isthmic spondylolisthesis (PIS) and the center of the L5 vertebra to obtain the 6DOF range of motion (ROM) at L4-L5 and the range of motion (ROM) between the AIS and the PIS. Relative motions of the cephalad vertebrae (ventral vertebrae) with respect to the caudad vertebrae (dorsal laminae) were analyzed using this coordinate system. Coordinates A and B represent the AIS and PIS of L4, respectively. X, Y, Z and X′, Y′, Z′ represented the primary planes of A and B. The X (X′) axis was set perpendicular to the anteroposterior axis to represent the left–right direction; the Y (Y′) axis was set perpendicular to the mediolateral axis to represent the anterior–posterior direction; and the Z (Z′) axis was set perpendicular to the transverse plane to represent the cranialcaudal direction. The rotations along the X, Y and Z axes were α, β, and γ, respectively [16–20].Fig. 3 Anatomical coordinate diagram of L4-5 isthmic spondylolisthesis: coordinate A was on the center of L4 vertebrae, coordinate B was on the posterior laminar of L4 isthmic spondylolisthesis. AIS indicates the anterior segment of isthmic spondylolisthesis, PIS indicates the posterior segment of isthmic spondylolisthesis

Statistical analysis

The continuous variables were measured as the mean ± SD, and an independent-samples t test was used to examine the differences in intervertebral translation and rotation at L4-5; a paired t test was used to examine the differences in intervertebral translation between the AIS and PIS. All analyses were performed using the Statistical Package for the Social Sciences (SPSS for Windows, release 19.0, IBM), and the significance level of P was set at 0.05.

Results

Intervertebral motions of L4-5 isthmic spondylolisthesis patients

The motion pattern at L4-5 with the IS was altered (Figs. 4, 5). During standing in the supine position, migration along the mediolateral axis was 4.90 ± 2.96 mm, which was greater than that of the control group (1.73 ± 1.10 mm) (P < 0.05). The extent of migration along the anteroposterior axis and the craniocaudal axis and the degree of rotation around the three axes were not significantly different between the treated group and the control group.Fig. 4 Ranges of intervertebral translation in patients among L4-5 IS and normal subjects around 3 principal axes under standing (A), flexion (B), twisting (C) and bending (D) of the torso. The symbols (*) represent statistical significance upon between-group (P < 0.05). IS indicates isthmic spondylolisthesis

Fig. 5 Ranges of intervertebral rotation in patients among L4-5 IS and normal subjects around 3 principal axes under standing (A), flexion (B), twisting (C) and bending (D) of the torso. The symbols (*) represent statistical significance upon between-group (P < 0.05). IS indicates isthmic spondylolisthesis

From flexion to extension, the migration along the mediolateral axis and the anteroposterior axis were 3.11 ± 1.86 mm and 2.45 ± 0.84 mm, respectively, which were greater than those of the control group at 1.43 ± 1.31 mm and 1.08 ± 1.05 mm, respectively (P < 0.05). Compared with those in the control group, migration along the craniocaudal axis and rotation around the three axes were not significantly different.

During left–right twisting, the migration along the mediolateral axis was 1.20 ± 1.30 mm, which was smaller than that of the control group (3.74 ± 1.73 mm; P < 0.05); however, the migration along the anteroposterior axis was 1.98 ± 0.87 mm, which was larger than that of the control group (0.99 ± 0.59 mm; P < 0.05). The rotation along the anteroposterior axis was 4.50° ± 2.26°, which was greater than that of the control group at 2.09° ± 1.83° (P < 0.05). Compared with those in the control group, migration along the craniocaudal axis and rotation of the mediolateral axis and the craniocaudal axis were not significantly different.

During left–right bending, the migration along the mediolateral axis was 1.85 ± 1.29 mm, which was lower than that of the control group (3.56 ± 2.14 mm; P < 0.05); however, the migration along the anteroposterior axis was 1.44 ± 0.76 mm, which was greater than that of the control group (0.63 ± 0.55 mm; P < 0.05). Compared with those in the control group, migration along the craniocaudal axis and rotation around the three axes were not significantly different.

Motion between the AIS and PIS

Comparing the AIS and PIS, the separation along the mediolateral axis in the standing, flexion and extension positions was 2.35 ± 1.71 mm, 2.80 ± 2.30 mm and 2.58 ± 2.14 mm, respectively, which were significantly greater than that in the supine position (0.50 ± 0.56 mm) (P < 0.05). The separation along the craniocaudal axis in the flexed position was 6.43 ± 3.41 mm, which was greater than that in the supine position (5.31 ± 3.34 mm) (P < 0.05). The separation along the anteroposterior axis in the flexion position was 42.97 ± 4.35 mm, which was greater than that in the standing position (41.79 ± 3.86 mm) (P < 0.05). There were no significant differences between the AIS and PIS groups and the control group (Table 2).Table 2 The Separation between AIS and PIS of L4 IS along the three planes (mean ± SD)

Postures		X (mm)	Y (mm)	Z (mm)	
SP-ST	SP	0.50 ± 0.56	41.16 ± 2.92	5.31 ± 3.34	
	ST	2.35 ± 1.71*	41.79 ± 3.86	5.41 ± 2.13	
SP-FL	SP	0.50 ± 0.56	41.16 ± 2.92	5.31 ± 3.34	
	FL	2.80 ± 2.30*	42.97 ± 4.35	6.43 ± 3.41*	
SP-EX	SP	0.50 ± 0.56	41.16 ± 2.92	5.31 ± 3.34	
	EX	2.58 ± 2.14*	41.40 ± 2.28	6.11 ± 2.77	
ST-FL	ST	2.35 ± 1.71	41.79 ± 3.86	5.41 ± 2.13	
	FL	2.80 ± 2.30	42.97 ± 4.35*	6.43 ± 3.41	
ST-EX	ST	2.35 ± 1.71	41.79 ± 3.86	5.41 ± 2.13	
	EX	2.58 ± 2.14	41.40 ± 2.28	6.11 ± 2.77	
FL-EX	FL	2.80 ± 2.30	42.97 ± 4.35	6.43 ± 3.41	
	EX	2.58 ± 2.14	41.40 ± 2.28	6.11 ± 2.77	
The symbols (*) represent statistical significance between different postures(P < 0.05)

SP: supine; ST: standing; FL: flexion; EX: extension; AIS: the anterior segment of isthmic spondylolisthesis; PIS: the posterior segment of isthmic spondylolisthesis

Discussion

The in vivo motion characteristics of vertebral segments with an IS are difficult to quantify in 6DOF, and few data have been reported in the literature. In this study, we used a combined MRI/CT and dual fluoroscopic imaging system to determine the motion patterns and ROMs of the vertebral segment with the IS in living patients under physiologic loading conditions and compared the data to those of normal subjects. The combined imaging technique was able to investigate all 6DOF motion with submillimetre/degree accuracy, which is particularly useful in study patients since sagittal motion alone may not fully describe the deformity and abnormal motion associated with spinal diseases [17]. In a study of lumbar segmental distribution, Mays et al. [23] reported that the incidences of L5, L4 and L3 were 48.3%, 24.1% and 10.7%, respectively, in 360 studied adult IS patients. In this study, the L4-5 IS, which has greater radiographic intelligibility than the L5-S1 IS because of the overlap of the ilium, was chosen as the research subject.

The motion characteristics of the IS

The test results showed that, for L4-5 IS patients, the translation along the anteroposterior axis at the flexion–extension, left–right bending and left–right twisting positions was greater than that of the control group. The rotation along the anteroposterior axis in the left–right twisting position was greater than that in the control group. However, the translation along the mediolateral axis presented paradoxical motion under different positions: at the left–right bending and left–right twisting positions, the relative translation was smaller than that of the control group, while at the supine-standing and flexion–extension positions, the relative translation was larger than that of the control group. Motion characteristics between the AIS and PIS: The relative separation of the AIS with respect to the PIS along the anteroposterior axis in the flexed position was significantly greater than that in the standing position. A decreasing trend but no significant change was found at the extension position. The separation of the AIS with respect to the PIS along the mediolateral axis in the standing, flexion and extension positions was significantly greater than that in the supine position.

Spinal instability, in particular, is considered a major cause of axial and radicular acute and chronic pain and is a frequent indication for surgery [15]. Some researchers have confirmed the existence of intervertebral instability in IS[3, 24, 25]. In a cadaveric kinematics study, Grobler et al. [24] reported that the instability of the L4-5 IS was worse than that of the L5-S1 IS and progressed significantly with time. Oh et al. [25] used flexion and extension radiographs to assess instability in patients with spondylolysis and reported that 15% of patients exhibited anterolisthesis, where flexion accentuated forward displacement, while an additional 15% of patients exhibited paradoxical motion. They concluded that patients without anterolisthesis during flexion in dynamic radiographs may still have (paradoxical) instability. By using positional MR in patients with spondylolysis and spondylolisthesis, Niggemann et al. [3] described a third form of instability (out of anterior and angular instabilities) defined as posterior instability that is not detectable by flexion–extension radiographs due to movements in the spondylolytic cleft. Posterior instability may lead to protrusion in the neuroforamen of a bony spur, flava ligaments or a cyst arising from the cleft itself with nerve root compression [3]. Other studies have shown that there may be no instability in IS [11, 26]. McGregor et al. [11] used MR imaging to investigate the relative displacement and intervertebral angular motion of lesion segments, and Axelsson et al. [26] used a roentgen stereophotogrammetric technique to assess the kinematics of the lumbar spine and demonstrated that a spondylolytic defect does not lead to detectable instability or hypermobility in the lumbar spine. Although patients with ISs lose fixation of posterior segments, this does not always lead to instability because the stability of the spine is affected by multiple factors. The facet joints only support one-third of spinal stabilization, while the muscles, ligaments and intervertebral discs might also play an important role in stabilizing the spine [27].

Nevertheless, an accurate definition of instability and the best diagnostic approach remain matters of debate and have given rise to controversy in the choice of the best treatment. These reported studies were conducted either in vitro or under nonphysiological loading conditions or focused on the study of motion in select planes. We quantified the in vivo motion characteristics of the vertebral segments with the IS in 6DOF and discovered the relative separation motion between the AIS and PIS. Compared with patients in the control group, symptomatic patients with IS exhibited intervertebral instability (3D instability) and especially presented paradoxical motion along the mediolateral axis due to differences in the laxity and tension of the annulus, capsules and ligaments at different positions [15, 25]. These outcomes were in accordance with those of an in vitro study using calf lumbar spines by Mihara et al. [28] and an in vivo study using positional MR by Niggemann et al. [3], which demonstrated that bilateral spondylolysis increased intervertebral mobility in flexion–extension. However, the patients with L4-5 IS in this study also showed greater intervertebral motion in other positions (supine standing, twisting, and bending).

Clinical significance of this study

Ischemic spondylolisthesis causes the vertebrae to split into two parts, and the motion characteristics might differ from those of degenerative spondylolisthesis because of the lack of rigid structural and facet joint constraints [4, 29]. This study revealed that left–right separation along the mediolateral axis from supine to standing and anterior–posterior separation along the anteroposterior axis from flexion to extension between the two parts directly decreased the possibility of compression of the spinal nerves. This phenomenon may account for the later clinical symptoms of IS patients [13].

Instability is an important factor in explaining clinical symptoms and determining surgical methods, such as decompression without fusion, posterolateral fusion with or without instrumentation and circumferential fusion [5, 30]. Dynamic X-ray imaging during flexion and extension is the most commonly used method in clinical practice and is widely recognized as an effective method for detecting the presence of lumbar segmental instability [31]. However, because these functional radiographs lack standardized routines and depend on the patient’s effort and cooperation, they can occasionally provide different results. Using standing lumbar X-rays (neutral, flexion, extension) and supine lumbar MRI, Lee et al. [32] found that ventral instability with symptomatic single-level lumbar spondylolisthesis was observed more frequently in the flexion-supine (79.5%) and neutral standing-supine (52.6%) groups than in the flexion–extension group (16.7%, P < 0.001). Morita et al. [33] found that the standing flexion–extension radiographs of a lumbar spondylolisthesis patient led by the hand demonstrated significantly greater sagittal translation, segmental angulation, and posterior opening and a greater rate of instability detection than those taken standardly without the patient being led by the hand. Therefore, we may underestimate instability in patients with single-level lumbar spondylolisthesis. All patients in this study had obvious symptoms, were not responsive to conservative treatment for 6 months and were eventually treated with surgery. The results quantitatively and qualitatively demonstrated the existence of 3D instability of the IS and the separation between the AIS and PIS at the lumbar spine during functional weight-bearing activities, providing a theoretical basis for the clinical treatment of adult ISs via surgery [3, 25].

There are certain limitations of this study. Our small sample size limited our ability to detect differences. This may also explain why some of the differences that were found were not statistically significant or why relatively large SDs were observed. A special pelvic limiter was applied to the hips of the participants while they performed active motions to minimize their hip motions to maximize lumbar spine motion. To maintain the targeted lumbar spine within the field view of the two fluoroscopes, the subject was instructed to limit flexion to approximately 45° from a standing position, not at the maximal flexion position of the subject. However, we were still able to observe statistical significance with respect to the number of tested subjects. Additionally, we only examined the range of motion of the L4-5 IS during the three functional body motions. Further investigations are necessary to enroll more patients and extend the results to general segments (L4-5, L5-S1) of the IS. This study only included individuals aged 50 to 60, lacking research on the elderly and adolescent populations. Additionally, this study was a single center study and lacked multi-center research.

Despite these limitations, the present study provided new data on motion characteristics in IS patients under various physiologic loading conditions.

In conclusion, this study utilized a novel combined imaging technique to investigate the 3D in vivo segmental motion characteristics of L4-5 and between dissociated segments of the IS during various functional postures. The results were compared with those of the normal subjects. In general, we found a larger ROM in patients with IS. These results also revealed and quantified the motion between the AIS and PIS at the lumbar spine during functional weight-bearing activities, primarily in the form of separation during flexion, which on average reached greater than 1 mm. Compared with patients in the control group, symptomatic patients with adult IS exhibited intervertebral instability, providing a theoretical basis for the clinical treatment of these patients during surgery.

Acknowledgements

The authors acknowledge the Imaging Department and Operation Department of the Mianyang Orthopedic Hospital, for their technical support and expertise in the radiological assessments. Meanwhile, the authors would like to express their gratitude to EditSprings (https://www.editsprings. cn) for the expert linguistic services provided.

Author contributions

Hongda Xu. Peidong Qing wrote the main manuscript text and Haitao Deng. Mingfan Li. Tieheng Wang prepared Figs. 1–5. Hongda Xu prepared Table 1.All authors reviewed the manuscript.

Funding

This project is supported by the National Natural Science Foundation of China (81371992).

Availability of data and materials

No datasets were generated or analysed during the current study.

Declarations

Ethics approval and consent to participate

Ethics committee approval by the Committee of the Mianyang Orthopedic Hospital (20240014).

Competing interests

The authors declare no competing interests.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
==== Refs
References

1. Kuligowski T Prevalence of lumbar segmental instability in young individuals with the different types of lumbar disc herniation-preliminary report Int J Environ Res Public Health 2022 19 15 9378 10.3390/ijerph19159378 35954735
Kuligowski T. Prevalence of lumbar segmental instability in young individuals with the different types of lumbar disc herniation-preliminary report. Int J Environ Res Public Health. 2022;19(15):9378. 10.3390/ijerph19159378.35954735 10.3390/ijerph19159378
2. Gopinath P Lumbar segmental instability: Points to ponder J Orthop 2015 12 4 165 167 10.1016/j.jor.2015.09.005 26566313
Gopinath P. Lumbar segmental instability: Points to ponder. J Orthop. 2015;12(4):165–7. 10.1016/j.jor.2015.09.005.26566313 10.1016/j.jor.2015.09.005
3. Niggemann P Kuchta J Beyer HK Grosskurth D Schulze T Delank KS Spondylolysis and spondylolisthesis: prevalence of different forms of instability and clinical implications Spine 2011 36 22 E1463 E1468 10.1097/BRS.0b013e3181d47a0e 20838368
Niggemann P, Kuchta J, Beyer HK, Grosskurth D, Schulze T, Delank KS. Spondylolysis and spondylolisthesis: prevalence of different forms of instability and clinical implications. Spine. 2011;36(22):E1463–8. 10.1097/BRS.0b013e3181d47a0e.20838368 10.1097/BRS.0b013e3181d47a0e
4. Wang Z Wang B Yin B Liu W Yang F Lv G The relationship between spinopelvic parameters and clinical symptoms of severe isthmic spondylolisthesis: a prospective study of 64 patients Eur Spine J 2014 23 3 560 568 10.1007/s00586-013-3064-2 24142043
Wang Z, Wang B, Yin B, Liu W, Yang F, Lv G. The relationship between spinopelvic parameters and clinical symptoms of severe isthmic spondylolisthesis: a prospective study of 64 patients. Eur Spine J. 2014;23(3):560–8. 10.1007/s00586-013-3064-2.24142043 10.1007/s00586-013-3064-2
5. Jones TR Rao RD Adult isthmic spondylolisthesis J Am Acad Orthop Surg 2009 17 10 609 617 10.5435/00124635-200910000-00003 19794218
Jones TR, Rao RD. Adult isthmic spondylolisthesis. J Am Acad Orthop Surg. 2009;17(10):609–17. 10.5435/00124635-200910000-00003.19794218 10.5435/00124635-200910000-00003
6. Dvorák J Panjabi MM Novotny JE Chang DG Grob D Clinical validation of functional flexion-extension roentgenograms of the lumbar spine Spine 1991 16 8 943 950 10.1097/00007632-199108000-00014 1835156
Dvorák J, Panjabi MM, Novotny JE, Chang DG, Grob D. Clinical validation of functional flexion-extension roentgenograms of the lumbar spine. Spine. 1991;16(8):943–50. 10.1097/00007632-199108000-00014.1835156 10.1097/00007632-199108000-00014
7. Pearcy M Shepherd J Is there instability in spondylolisthesis? Spine 1985 10 2 175 177 10.1097/00007632-198503000-00014 4002042
Pearcy M, Shepherd J. Is there instability in spondylolisthesis? Spine. 1985;10(2):175–7. 10.1097/00007632-198503000-00014.4002042 10.1097/00007632-198503000-00014
8. Friberg O Instability in spondylolisthesis Orthopedics 1991 14 4 463 465 10.3928/0147-7447-19910401-11 2038581
Friberg O. Instability in spondylolisthesis. Orthopedics. 1991;14(4):463–5. 10.3928/0147-7447-19910401-11.2038581 10.3928/0147-7447-19910401-11
9. Fayyazi AH Ordway NR Park SA Fredrickson BE Yonemura K Yuan HA Radiostereometric analysis of postoperative motion after application of dynesys dynamic posterior stabilization system for treatment of degenerative spondylolisthesis J Spinal Disord Tech 2010 23 4 236 241 10.1097/BSD.0b013e3181a4bb0b 20072031
Fayyazi AH, Ordway NR, Park SA, Fredrickson BE, Yonemura K, Yuan HA. Radiostereometric analysis of postoperative motion after application of dynesys dynamic posterior stabilization system for treatment of degenerative spondylolisthesis. J Spinal Disord Tech. 2010;23(4):236–41. 10.1097/BSD.0b013e3181a4bb0b.20072031 10.1097/BSD.0b013e3181a4bb0b
10. Niggemann P Kuchta J Hadizadeh D Pieper CC Schild HH Classification of spondylolytic clefts in patients with spondylolysis or isthmic spondylolisthesis using positional MRI Acta Radiol 2017 58 2 183 189 10.1177/0284185116638566 26987671
Niggemann P, Kuchta J, Hadizadeh D, Pieper CC, Schild HH. Classification of spondylolytic clefts in patients with spondylolysis or isthmic spondylolisthesis using positional MRI. Acta Radiol. 2017;58(2):183–9. 10.1177/0284185116638566.26987671 10.1177/0284185116638566
11. McGregor AH Anderton L Gedroyc WM Johnson J Hughes SP The use of interventional open MRI to assess the kinematics of the lumbar spine in patients with spondylolisthesis Spine 2002 27 14 1582 1586 10.1097/00007632-200207150-00019 12131722
McGregor AH, Anderton L, Gedroyc WM, Johnson J, Hughes SP. The use of interventional open MRI to assess the kinematics of the lumbar spine in patients with spondylolisthesis. Spine. 2002;27(14):1582–6. 10.1097/00007632-200207150-00019.12131722 10.1097/00007632-200207150-00019
12. Alfieri A Gazzeri R Prell J Röllinghoff M The current management of lumbar spondylolisthesis J Neurosurg Sci 2013 57 2 103 113 23676859
Alfieri A, Gazzeri R, Prell J, Röllinghoff M. The current management of lumbar spondylolisthesis. J Neurosurg Sci. 2013;57(2):103–13.23676859
13. Leone A Cianfoni A Cerase A Magarelli N Bonomo L Lumbar spondylolysis: a review Skeletal Radiol 2011 40 6 683 700 10.1007/s00256-010-0942-0 20440613
Leone A, Cianfoni A, Cerase A, Magarelli N, Bonomo L. Lumbar spondylolysis: a review. Skeletal Radiol. 2011;40(6):683–700. 10.1007/s00256-010-0942-0.20440613 10.1007/s00256-010-0942-0
14. Alyas F Connell D Saifuddin A Upright positional MRI of the lumbar spine Clin Radiol 2008 63 9 1035 1048 10.1016/j.crad.2007.11.022 18718234
Alyas F, Connell D, Saifuddin A. Upright positional MRI of the lumbar spine. Clin Radiol. 2008;63(9):1035–48. 10.1016/j.crad.2007.11.022.18718234 10.1016/j.crad.2007.11.022
15. Izzo R Guarnieri G Guglielmi G Muto M Biomechanics of the spine. Part II: spinal instability Eur J Radiol 2013 82 1 127 138 10.1016/j.ejrad.2012.07.023 23088878
Izzo R, Guarnieri G, Guglielmi G, Muto M. Biomechanics of the spine. Part II: spinal instability. Eur J Radiol. 2013;82(1):127–38. 10.1016/j.ejrad.2012.07.023.23088878 10.1016/j.ejrad.2012.07.023
16. Bai JQ Hu YC Assessing validation of dual fluoroscopic image matching method for measurement of in vivo spine kinematics Chin Med J 2011 124 11 1689 1694 21740779
Bai JQ, Hu YC, et al. Assessing validation of dual fluoroscopic image matching method for measurement of in vivo spine kinematics. Chin Med J. 2011;124(11):1689–94.21740779
17. Miao J Wang S Park WM Segmental spinal canal volume in patients with degenerative spondylolisthesis Spine J 2013 13 6 706 712 10.1016/j.spinee.2013.02.017 23541448
Miao J, Wang S, Park WM, et al. Segmental spinal canal volume in patients with degenerative spondylolisthesis. Spine J. 2013;13(6):706–12. 10.1016/j.spinee.2013.02.017.23541448 10.1016/j.spinee.2013.02.017
18. Xu H, Liu J, Li H, Wei D, Miao J, Xia Q. Zhongguo Xiu Fu Chong Jian Wai Ke Za Zhi. 2018;32(12):1560–1566. 10.7507/1002-1892.201807026.
19. Xia Q Wang S Kozanek M Passias P Wood K Li G In-vivo motion characteristics of lumbar vertebrae in sagittal and transverse planes J Biomech 2010 43 10 1905 1909 10.1016/j.jbiomech.2010.03.023 20381051
Xia Q, Wang S, Kozanek M, Passias P, Wood K, Li G. In-vivo motion characteristics of lumbar vertebrae in sagittal and transverse planes. J Biomech. 2010;43(10):1905–9. 10.1016/j.jbiomech.2010.03.023.20381051 10.1016/j.jbiomech.2010.03.023
20. Miao J Wang S Wan Z Motion characteristics of the vertebral segments with lumbar degenerative spondylolisthesis in elderly patients Eur Spine J 2013 22 2 425 431 10.1007/s00586-012-2428-3 22892705
Miao J, Wang S, Wan Z, et al. Motion characteristics of the vertebral segments with lumbar degenerative spondylolisthesis in elderly patients. Eur Spine J. 2013;22(2):425–31. 10.1007/s00586-012-2428-3.22892705 10.1007/s00586-012-2428-3
21. Jesse CM Schwarzenbach O Ulrich CT Häni L Raabe A Schär RT Safety and efficacy of stand-alone anterior lumbar interbody fusion in low-grade L5–S1 isthmic spondylolisthesis Brain Spine 2022 2 100861 10.1016/j.bas.2022.100861 36248123
Jesse CM, Schwarzenbach O, Ulrich CT, Häni L, Raabe A, Schär RT. Safety and efficacy of stand-alone anterior lumbar interbody fusion in low-grade L5–S1 isthmic spondylolisthesis. Brain Spine. 2022;2:100861. 10.1016/j.bas.2022.100861.36248123 10.1016/j.bas.2022.100861
22. Xia Q Wang S Passias PG In vivo range of motion of the lumbar spinous processes Eur Spine J 2009 18 9 1355 1362 10.1007/s00586-009-1068-8 19543753
Xia Q, Wang S, Passias PG, et al. In vivo range of motion of the lumbar spinous processes. Eur Spine J. 2009;18(9):1355–62. 10.1007/s00586-009-1068-8.19543753 10.1007/s00586-009-1068-8
23. Mays S Spondylolysis, spondylolisthesis, and lumbo-sacral morphology in a medieval English skeletal population Am J Phys Anthropol 2006 131 3 352 362 10.1002/ajpa.20447 16634047
Mays S. Spondylolysis, spondylolisthesis, and lumbo-sacral morphology in a medieval English skeletal population. Am J Phys Anthropol. 2006;131(3):352–62. 10.1002/ajpa.20447.16634047 10.1002/ajpa.20447
24. Grobler LJ Novotny JE Wilder DG Frymoyer JW Pope MH L4–5 isthmic spondylolisthesis. A biomechanical analysis comparing stability in L4–5 and L5–S1 isthmic spondylolisthesis Spine 1994 19 2 222 227 10.1097/00007632-199401001-00018 8153834
Grobler LJ, Novotny JE, Wilder DG, Frymoyer JW, Pope MH. L4–5 isthmic spondylolisthesis. A biomechanical analysis comparing stability in L4–5 and L5–S1 isthmic spondylolisthesis. Spine. 1994;19(2):222–7.8153834 10.1097/00007632-199401001-00018
25. Oh JY Liang S Louange D Rahmat R Hee HT Kumar VP Paradoxical motion in L5–S1 adult spondylolytic spondylolisthesis Eur Spine J 2012 21 2 262 267 10.1007/s00586-011-1880-9 21674210
Oh JY, Liang S, Louange D, Rahmat R, Hee HT, Kumar VP. Paradoxical motion in L5–S1 adult spondylolytic spondylolisthesis. Eur Spine J. 2012;21(2):262–7. 10.1007/s00586-011-1880-9.21674210 10.1007/s00586-011-1880-9
26. Axelsson P Johnsson R Strömqvist B Is there increased intervertebral mobility in isthmic adult spondylolisthesis? A matched comparative study using roentgen stereophotogrammetry Spine 2000 25 13 1701 1703 10.1097/00007632-200007010-00014 10870146
Axelsson P, Johnsson R, Strömqvist B. Is there increased intervertebral mobility in isthmic adult spondylolisthesis? A matched comparative study using roentgen stereophotogrammetry. Spine. 2000;25(13):1701–3. 10.1097/00007632-200007010-00014.10870146 10.1097/00007632-200007010-00014
27. Sharma M Langrana NA Rodriguez J Role of ligaments and facets in lumbar spinal stability Spine 1995 20 8 887 900 10.1097/00007632-199504150-00003 7644953
Sharma M, Langrana NA, Rodriguez J. Role of ligaments and facets in lumbar spinal stability. Spine. 1995;20(8):887–900. 10.1097/00007632-199504150-00003.7644953 10.1097/00007632-199504150-00003
28. Mihara H Onari K Cheng BC David SM Zdeblick TA The biomechanical effects of spondylolysis and its treatment Spine 2003 28 3 235 238 10.1097/01.BRS.0000042226.59713.0E 12567023
Mihara H, Onari K, Cheng BC, David SM, Zdeblick TA. The biomechanical effects of spondylolysis and its treatment. Spine. 2003;28(3):235–8. 10.1097/01.BRS.0000042226.59713.0E.12567023 10.1097/01.BRS.0000042226.59713.0E
29. Jeong HY You JW Sohn HM Park SH Radiologic evaluation of degeneration in isthmic and degenerative spondylolisthesis Asian Spine J 2013 7 1 25 33 10.4184/asj.2013.7.1.25 23508359
Jeong HY, You JW, Sohn HM, Park SH. Radiologic evaluation of degeneration in isthmic and degenerative spondylolisthesis. Asian Spine J. 2013;7(1):25–33. 10.4184/asj.2013.7.1.25.23508359 10.4184/asj.2013.7.1.25
30. Sengupta DK Herkowitz HN Degenerative spondylolisthesis: review of current trends and controversies Spine 2005 30 6 Suppl S71 S81 10.1097/01.brs.0000155579.88537.8e 15767890
Sengupta DK, Herkowitz HN. Degenerative spondylolisthesis: review of current trends and controversies. Spine. 2005;30(6 Suppl):S71–81. 10.1097/01.brs.0000155579.88537.8e.15767890 10.1097/01.brs.0000155579.88537.8e
31. Wang Y Huang K Research progress of diagnosing methodology for lumbar segmental instability: A narrative review Medicine (Baltimore) 2022 101 1 e28534 10.1097/MD.0000000000028534 35029921
Wang Y, Huang K. Research progress of diagnosing methodology for lumbar segmental instability: A narrative review. Medicine (Baltimore). 2022;101(1):e28534. 10.1097/MD.0000000000028534.35029921 10.1097/MD.0000000000028534
32. Lee NJ Mathew J Kim JS Flexion-extension standing radiographs underestimate instability in patients with single-level lumbar spondylolisthesis: comparing flexion-supine imaging may be more appropriate J Spine Surg 2021 7 1 48 54 10.21037/jss-20-631 33834127
Lee NJ, Mathew J, Kim JS, et al. Flexion-extension standing radiographs underestimate instability in patients with single-level lumbar spondylolisthesis: comparing flexion-supine imaging may be more appropriate. J Spine Surg. 2021;7(1):48–54. 10.21037/jss-20-631.33834127 10.21037/jss-20-631
33. Morita T Yoshimoto M Terashima Y Do we have adequate flexion-extension radiographs for evaluating instability in patients with lumbar spondylolisthesis? Spine 2020 45 1 48 54 10.1097/BRS.0000000000003203 31415456
Morita T, Yoshimoto M, Terashima Y, et al. Do we have adequate flexion-extension radiographs for evaluating instability in patients with lumbar spondylolisthesis? Spine. 2020;45(1):48–54. 10.1097/BRS.0000000000003203.31415456 10.1097/BRS.0000000000003203
