Prevalence and Risk Factors of Degenerative Spondylolisthesis and Retrolisthesis in the Thoracolumbar and Lumbar Spine – An EOS Study Using Updated Radiographic Parameters

Abstract

Study design

Single centre, cross-sectional study.

Objectives

The objective is to report the prevalence of spondylolisthesis and retrolisthesis, analyse both conditions in terms of the affected levels and severity, as well as identify their risk factors.

Methods

A review of clinical data and radiographic images of consecutive spine patients seen in outpatient clinics over a 1-month period is performed. Images are obtained using the EOS® technology under standardised protocol, and radiographic measurements were performed by 2 independent, blinded spine surgeons. The prevalence of both conditions were shown and categorised based on the spinal level involvement and severity. Associated risk factors were identified.

Results

A total of 256 subjects (46.1% males) with 2304 discs from T9/10 to L5/S1 were studied. Their mean age was 52.2(± 18.7) years. The overall prevalence of spondylolisthesis and retrolisthesis was 25.9% and 17.1% respectively. Spondylolisthesis occurs frequently at L4/5(16.3%), and retrolisthesis at L3/4(6.8%). Majority of the patients with spondylolisthesis had a Grade I slip (84.3%), while those with retrolisthesis had a Grade I slip. The presence of spondylolisthesis was found associated with increased age (P < .001), female gender (OR: 2.310; P = .005), predominantly sitting occupations (OR:2.421; P = .008), higher American Society of Anaesthesiology grades (P = .001), and lower limb radiculopathy (OR: 2.175; P = .007). Patients with spondylolisthesis had larger Pelvic Incidence (P < .001), Pelvic Tilt (P < .001) and Knee alignment angle (P = .011), but smaller Thoracolumbar junctional angle (P = .008), Spinocoxa angle (P = .007). Retrolisthesis was associated with a larger Thoracolumbar junctional angle (P =.039).

Conclusion

This is the first study that details the prevalence of spondylolisthesis and retrolisthesis simultaneously, using the EOS technology and updated sagittal radiographic parameters. It allows better understanding of both conditions, their mutual relationship, and associated clinical and radiographic risk factors.

Keywords

spondylolisthesis retrolisthesis eos imaging radiography sagittal radiographic parameters

Highlights

1. The prevalence of spondylolisthesis and retrolisthesis was 25.9% and 17.1% respectively. Spondylolisthesis occurs frequently at L4/5 (16.3%), and retrolisthesis at L3/4 (6.8%). Majority of the patients with spondylolisthesis had a Grade I slip (84.3%), while all those with retrolisthesis had a Grade I slip.

2. The presence of spondylolisthesis was found to be associated with increased age of subject (p < 0.001), female gender (OR 2.310; p = 0.005), predominantly sitting occupations (OR = 2.421; P = 0.008, higher American Society of Anaesthesiology grades (P = 0.001), and lower limb radiculopathy (OR = 2.175; P = 0.007).

3. Patients with spondylolisthesis had larger Pelvic Incidence (P < 0.001), Pelvic Tilt (P < 0.001), and Knee alignment angle (P = 0.011), but smaller Thoracolumbar junctional angle (P = 0.008), and Spinocoxa angle (P = 0.007), while retrolisthesis was associated with a larger Thoracolumbar junctional angle (P = 0.039). These findings likely reflect the primary pathology and compensatory mechanisms in whole body balancing.

4. Associations between level-specific spinopelvic parameters lumbar incidence, lumbar tilt, and lumbar slope and vertebral translations at the corresponding levels reflect the importance of recognizing force mechanics in the spine.

5. The use of EOS technology and updated sagittal radiographic parameters in this study allowed the understanding of both conditions, their mutual relationship, and associated clinical and radiographic risk factors. It will lay the platform for future management of both conditions.

Introduction

Spondylolisthesis and retrolisthesis describe the forward and backward translation of a vertebra with reference to its adjacent lower vertebra respectively. While the epidemiology and pathophysiology of spondylolisthesis may have been extensively studied^1-3, retrolisthesis is less known⁴. This could be due to a relatively lower prevalence^5,6, or its more quiescent nature which results in a paucity of evidence demonstrating its clinical significance⁶. The underlying causes for both conditions may differ⁷, hence resulting in them often being studied separately. However, both conditions require a nett force to translate one vertebra over another, which may indicate that biomechanically these 2 conditions may be related. Therefore, it would be necessary to report the prevalence of both conditions together, and document their clinical and radiological risk factors.

The rapidly evolving concepts in adult spinal deformity surgery have highlighted the importance of realigning the sagittal profile of the spine^8,9. Considerations in spinal realignment include assessment of a deformity using the sagittal vertical axis (SVA), and the pelvic incidence (PI) – lumbar lordosis (LL) discrepancy, as well as appreciating the extent of spinopelvic compensation using the pelvic tilt (PT)^9,10. Retrolisthesis, which was once regarded as a possible form of spinal instability of unknown significance¹¹, is now being increasingly recognized today as a compensatory process which occurs in patients with positive sagittal imbalance^9,11. With a greater forward lean of the spine in ageing, or following various spinal pathologies, retrolisthesis may occur in an attempt to keep the body balance within the cone of economy^12,13.

To our knowledge, this is the first epidemiological study that investigates the prevalence of spondylolisthesis and retrolisthesis simultaneously using the modern EOS® technology, which is the current gold standard modality for taking true-to-proportion and true-to-axis whole body images for the assessment of spinal alignment^14,15. Although previous studies have reported on the epidemiology of these conditions, no prior study have been carried out to investigate their relationship with whole body radiographic parameters, which is pivotal in the understanding of adult spinal deformity today. This study also aims to identify associated clinical and updated radiological risk factors in both conditions.

Methodology

Study Design

This was a single centre, cross-sectional study on the prevalence of degenerative spondylolisthesis and retrolisthesis in the thoracolumbar and lumbar spine using the EOS® technology (EOS® imaging, Paris, France)¹⁶, with identification of associated risk factors. All images within the centre were obtained using the EOS® technology. This study is approved by the local ethics board committee. Informed consent was obtained from each patient for inclusion in the study.

Study Population

We enrolled all first visit patients seen at the spine centre over a 1-month period. Patients with spinal scoliosis, either diagnosed clinically by a positive Adam’s forward bend test, or radiologically with coronal Cobb angle measurements >10° shown on EOS, were excluded from the study sample. This is to avoid misinterpretation of sagittal and coronal plane deformities due to spinal rotation. As a result, a total of 256 subjects (136 women and 120 men) out of 275 were enrolled.

Radiographic Examination

Following clinical assessment by the attending spine specialist, all subjects underwent anteroposterior and lateral whole body radiographs using EOS® technology. This technology is the current gold standard modality for taking true-to-proportion and true-to-axis whole body images for the accurate assessment of spinal alignment ^14,15.

To promote standardization, pictorial charts demonstrating how to position for the EOS imaging were displayed by the EOS® machine. Uniformity of this posture was further reinforced through standardized verbal instructions given by the radiographer as follows: “stand as straight as possible without leaning forwards or backwards, and touch your collarbones with your fingers”. All images were performed by trained radiographers with over 3 years of experience in EOS® technology.

Data Collection

A review of electronic medical case records was conducted for all patients identified in the study. Clinical data obtained include patient demography (age, gender, ethnicity, occupation), American Society of Anaesthesiology (ASA) Physical Status Classification, and symptomology (presence of previous or ongoing axial back pain or lower limb radiculopathy). The subjects’ occupations were categorised into ‘predominantly standing’ or ‘predominantly sitting’.

Radiographic Measurements

The radiographs obtained were stored on the hospital’s secured server and accessed using Centricity Enterprise Web version 3.0 (GE Medical Systems Information Technologies, Barrington, IL, USA) for measurements of spinal parameters. Measurements were performed by 2 independent and blinded spine surgeons, and an average of their readings was recorded.

Vertebral translation was deemed to be present if the translation was measured to be ≥3mm. The radiographic outcomes measures include: 1. Presence or absence of spondylolisthesis and retrolisthesis; 2. The level affected; 3. Severity assessment of both conditions using Meyerding’s classification . Other radiographical covariates measured can be divided into 4 main categories of assessment and include: 1. Global spinal alignment; 2. Regional spinal angles; 3. Spinopelvic angles, and 4. Lower limb angles.

For global spinal alignment, Sagittal Vertical Axis (SVA) was measured as the horizontal offset between the imaginary sagittal C7 plumb line and the posterosuperior corner of the S1 vertebral body. T12SVA measures a similar offset but uses an imaginary plumb line from T12 instead.

For regional spinal alignment, thoracic and lumbar spinal curvatures were performed using the Cobb method. Global thoracic angle (GTA) was taken as the angle between the superior endplate of T1and the superior endplate of T12. Thoracolumbar junctional angle (TLA) was taken as the angle between the superior endplate of T10 and the inferior endplate of L2. Global lumbar angle (GLA) was taken as the inferior endplate of T12 and the superior endplate of S1.

Spinopelvic parameters such as PI, PT and SS, as well as T1-slope were measured using standard methods described in the literature. To ascertain the individual relationship between the vertebra alignment and the hip, the spatial orientation of each vertebra is assessed using lumbar incidence (LI), lumbar tilt (LT) and lumbar slope (LS) as proposed by Hey et al¹⁷. This is conceptually identical to the PI, PT and SS used for S1 vertebra, such that LI = LT + LS for any given lumbar vertebra.

Femoral alignment angle (FAA) was taken as the acute angle subtended by the femoral axis (midpoint of bicoxafemoral hip center to midpoint of both mid-Blumensaat lines) and the vertical axis (see Figure 1). Knee alignment angle (KAA) was taken as the acute angle between the femoral axis and the tibia axis (midpoint of both mid-tibia plateau to the midpoint of both mid-tibia plafond). Spinocoxa angle (SCA), was taken as the acute angle subtended by the perpendicular to the superior endplate of the inflection vertebra and the femoral axis. The inflection vertebra is defined as the most tilted vertebra on the lateral EOS® image that marks the distal end of the kyphosis and proximal end of the lordosis at the thoracolumbar junction. It is used for the measurements of SCA and Inflection to S1 angle (IL).

Figure 1.

Sketch diagram showing the differences in sagittal alignment parameters between patients with and without spondylolisthesis.

Statistical Analysis

Data collected was compiled in Microsoft Excel 2011 (Version 14.2.4). Two-sided statistical analysis was carried out using Statistical Package for the Social Sciences version 22.0 with significance set at P<.05. Categorical variables are described in percentages and continuous variables as means with standard deviations.

The prevalence of both spondylolisthesis and retrolisthesis, their involved spinal levels and severities were presented. Their associations with the other clinical and radiological parameters were also analysed using univariate Chi Squared and Fisher Exact Test for categorical variables, Mann-Whitney U Test for ordinal variables and, Independent-Samples t-Test for continuous variables.

Results

Sample Characteristics

A total of 256 subjects (46.1% males and 53.9% females) with 2304 discs from T9/10 to L5/S1 were studied. Their mean age was 52.2 (± 18.7) years (Table 1).

Table 1.

Overall population sample characteristics

Characteristic	Mean (n = 256)	Percentages
^aAge (years)	52.2	18.7
Gender
Males	118	46.1
Females	138	53.9
Ethnicity
Chinese	191	74.6
Malay	21	8.2
Indian	22	8.6
Others	22	8.6
Occupation
Predominant sitting	167	65.2
Predominant standing	89	34.8
ASA Grade
Grade I	114	44.5
Grade II	124	48.4
Grade III	18	7.0
Symptomology
Low Back Pain	167	65.5
Lower Limb Radiculopathy	111	43.5

^a Age is presented as mean with 1SD.

Statistically significant results.

The most common ethnic group was Chinese (74.6%), which is consistent with the nation’s population demographics. The majority of subjects (65.2%) had predominantly sitting occupations. 92.9% of the subjects had ASA grade of Grade I-II. (Table 1). 65.5% and 43.5% of the population have symptoms of low back pain and lower limb radiculopathy respectively.

Prevalence of Spondylolisthesis and Retrolisthesis

The occurrence of thoracolumbar and lumbar spondylolisthesis and retrolisthesis in the study population was 25.8% and 17.2% respectively (Table 2). 10 patients (.04%) presented with both spondylolisthesis and retrolisthesis. 3 patients have multilevel spondylolisthesis involving the adjacent cranial vertebra, and none has skipped level spondylolisthesis. 8 patients have multilevel retrolisthesis, of which 6 had adjacent vertebra, and 2 had skipped level involvement.

Table 2.

Prevalence of Thoracolumbar and Lumbar Spondylolisthesis and Retrolisthesis by spinal levels

Spinal Levels	Presence of spondylolisthesis	Prevalence of Spondylolisthesis, %	Presence of retrolisthesis	Prevalence of Retrolisthesis, %
T9/10	1	0.4	0	0.0
T10/11	2	0.8	0	0.0
T11/12	1	0.4	0	0.0
T12/L1	0	0.0	1	0.4
L1/2	0	0.0	14	5.5
L2/3	5	2.0	9	3.5
L3/4	12	4.7	18	7.0
L4/5	42	16.4	5	2.0
L5/S1	9	3.5	6	2.3
Overall	66	25.8 (95% CI 20 – 31)	44	17.2 (95% CI 13 – 22)

In terms of the level involved, spondylolisthesis occurs frequently at L4/5 (16.4%), followed by L3/4 (4.7%) and L5/S1 (3.5%). Retrolisthesis is more common at L3/4 (7.0%) followed by L1/2 (5.5%) and L2/3 (3.5%) (Table 2). 84.3% of the spondylolisthesis are Grade I (Meyerding’s classification) while the remaining 15.7% are Grade II. All retrolisthesis are classified as Grade I.

Clinical Characteristics of Patients With Spondylolisthesis and Retrolisthesis

The mean age of subjects with spondylolisthesis was 62.8(± 12.5) years while the mean age of subjects without spondylolisthesis was 48.0(± 18.8) years. The mean age of subjects with retrolisthesis was 57.0 (± 16.6) years while the mean age of subjects without retrolisthesis was 50.7(± 18.8) years. Age-stratified prevalence showed a sudden increase in spondylolisthesis beyond 50 years old and a slow, gradual increase for retrolisthesis (Table 3).

Table 3.

Relationship between patient characteristics (stratified) and the prevalence of spondylolisthesis and retrolisthesis

Characteristic	Number of subjects (n = 256)	Presence of Spondylolisthesis (%)	Odds Ratio (CI)	p	Presence of Retrolisthesis (%)	Odds Ratio (CI)	p
Age				< .001 *			.231
<20	16	0 (.0)	-		2 (12.5)	-
20 – 30	28	3 (10.7)	4.53 (.22 – 93.49)		3 (10.7)	.84 (.13 – 5.64)
30 – 40	31	1 (3.2)	1.62 (.06 – 42.12)		1 (3.2)	.23 (.02 – 2.79)
40 – 50	38	4 (10.5)	4.30 (.22 – 84.75)		8 (21.1)	1.87 (.35 – 9.96)
50 – 60	36	12 (33.3)	16.84 (.93 – 304.42)		8 (22.9)	2.00 (.37 – 10.70)
60 – 70	63	24 (38.1)	20.47 (1.17 – 356.81)		11 (18.0)	1.48 (.29 – 7.47)
>70	44	23 (52.3)	36.07 (2.04 – 638.52)		10 (23.8)	2.06 (.40 – 10.62)
Gender				.005 *			.367
Male	118	21 (17.8)	-		23 (19.5)	-
Female	138	46 (33.3)	2.310 (1.281 – 4.165)		21 (15.2)	.741 (.387 – 1.421)
Ethnicity				.295			.790
Chinese	191	53 (27.7)	-		34 (17.8)	-
Malay	21	5 (23.8)	.814 (.284 – 2.332)		4 (19.0)	1.087 (.344 – 3.433)
Indian	22	2 (9.1)	.260 (.059 – 1.153)		2 (9.1)	.462 (.103 – 2.070)
Others	22	6 (27.3)	.976 (.363 – 2.629)		4 (18.2)	1.026 (.327 – 3.225)
Occupation				.008 *			.918
Predominant Standing	89	14 (15.9)	-		29 (17.4)	-
Predominant Sitting	167	52 (31.2)	2.421 (1.255 – 4.673)		15 (17.0)	.965 (.487 – 1.912)
ASA Grade				.001 *			.634
Grade I	114	18 (15.8)	-		17 (14.9)	-
Grade II	124	40 (32.3)	2.540 (1.354 – 4.762)		24 (19.4)	1.369 (.693 – 2.706)
Grade III	18	9 (50.0)	5.333 (1.862 – 15.274)		3 (16.7)	1.141 (.298 – 4.369)
Symptomology
Low back pain	167	41 (24.4)	.770 (.432 – 1.372)	.375	27 (16.1)	.800 (.409 – 1.564)	.514
Lower limb Radiculopathy	111	38 (34.2)	2.175 (1.231 – 3.842)	.007 *	17 (15.3)	.827 (.424 – 1.615)	.579

Statistically significant results.

The presence of spondylolisthesis was found to be associated with increased age of subject (P<.001), female gender (OR 2.31; P=.005), predominantly sitting occupations (OR = 2.42; P=.008) (Table 3). In addition, compared to patients with ASA Grade I, Grade II and III patients have an increased association with spondylolisthesis (P=.001). No significant differences were found between the occurrence of spondylolisthesis and patient ethnicity.

Axial symptoms correlate poorly with spondylolisthesis and retrolisthesis. However, lower limb radiculopathy was found to be associated with lumbar spondylolisthesis (OR = 2.18; P=.007). No significant associations were found for retrolisthesis.

Radiological Characteristics of Patients With Spondylolisthesis and Retrolisthesis

Patients with spondylolisthesis had larger PI (P<.001), PT (P<.001) and KAA (P=.011), but smaller TLA (P=.008) and SCA (P=.007) (Table 4). Retrolisthesis associated with a larger TLA (P=.039).

Table 4.

Relationship between radiological parameters and the prevalence of spondylolisthesis and retrolisthesis

Parameters	Total	Presence of Spondylolisthesis	Absence of Spondylolisthesis	p	Presence of Retrolisthesis	Absence of Retrolisthesis	p
Spinal Balance, cm
C0SVA,	3.1 ± 2.7	3.2 ± 2.5	3.1 ± 2.7	.856	2.8 ± 2.6	3.2 ± 2.7	.365
C7SVA	2.8 ± 2.6	2.9 ± 2.3	2.9 ± 2.7	.979	2.8 ± 2.7	2.9 ± 2.5	.936
Spinal angles, °
T1 Slope	19.5 ± 10.0	17.6 ± 11.4	20.2 ± 9.5	.165	18.0 ± 10.3	19.9 ± 10.0	.307
GTA	35.2 ± 13.5	32.6 ±14.3	36.0 ± 13.2	.135	32.7 ± 14.7	35.7 ± 13.2	.232
TLA	10.9 ± 9.7	8.6 ± 7.0	11.7 ± 10.4	.008 *	14.4 ± 11.8	10.3 ± 9.2	.039 *
GLA	48.1 ± 15.2	49.9 ± 14.7	47.5 ± 15.4	.275	45.7 ± 15.3	48.6 ± 15.2	.269
IL	48.0 ± 14.1	48.8 ± 14.4	47.8 ± 14.1	.642	48.2 ± 13.3	48.0 ± 14.3	.934
Spinopelvic angles
PI	53.4 ± 11.8	59.3 ± 12.0	51.3 ± 11.0	<.001 *	54.5 ± 11.8	53.1 ± 11.8	.532
PT	20.1 ± 9.8	24.6 ± 9.6	18.6 ± 9.4	<.001 *	22.8 ± 9.4	19.6 ± 9.8	.052
SS	32.4 ±10.5	34.0 ± 9.8	31.8 ± 10.7	.147	30.2 ± 10.4	32.8 ± 10.5	.154
Lower limb angles
FAA	3.1 ± 3.5	2.4 ± 3.2	3.3 ± 3.6	.061	3.4 ± 3.4	3.0 ± 3.5	.548
SCA	21.1 ± 8.4	18.6 ± 8.4	21.9 ± 8.2	.007 *	22.4 ± 7.7	20.8 ± 8.5	.283
KAA	2.0 ± 6.5	3.8 ± 5.9	1.3 ± 6.6	.011 *	2.3 ± 6.6	1.9 ± 6.5	.710

All values are presented as means (± 1SD)

In terms of level-specific spinopelvic parameters and their association with spondylolisthesis and retrolisthesis at the said level, larger L4I and L4S were associated with L3/4 spondylolisthesis (P=.003 and P=.045 respectively) and absence of L3/4 retrolisthesis is associated with L4S (P=.011) but not L4I (P=.062). Larger L5I (P<.001), L5T (P=.001) and L5S (P=.015) were associated with L4/5 spondylolisthesis. A larger SS is associated with absence of retrolisthesis (P=.033).

Discussion

Spondylolisthesis and retrolisthesis describe abnormal vertebral translations of the spine in the sagittal plane. The former occurs when a vertebra body translates forward over its caudal counterpart, and the latter occurs with backward translation. Generally, spondylolisthesis is perceived as abnormal, and may lead to symptoms such as back pain and/or leg pain^18,19. Hypermobility of the affected segments, which can be further assessed using stress radiography²⁰ or MRI²¹, can result in a wide range of clinical presentations²². Several radiological parameters that predict the progression of spondylolisthesis, can be used to guide management –1) the slip angle which essentially measures the angle difference between endplates of 2 involved vertebra^23,24, 2) the sacral inclination which can be regarded as a variant of the slip angle as it uses the longitudinal axis of the sacrum instead of the superior endplate²³, and 3) the lumbosacral angle aka sacral slope²⁵. In the presence of symptoms that are refractory to conservative management, especially in patients with high risk of disease progression, surgery is often necessary²⁵. The recommended surgery involves decompression of neural structures with or without instrumented fusion of the affected spinal segment^26,27. This has been shown in the SPORT trial to demonstrate superior results compared to non-operative management up to 4 years²⁸.

The prevalence of spondylolisthesis in the general population has been reported to be between 6 to 10%, and varies depending on the type of spondylolisthesis and imaging modality used^29,30. The prevalence of this condition in a random community sample via non-weight bearing CT studies was found to be 11.5%³¹. In our study, the prevalence was expectedly higher (25.8%) due to our population sample which recruits pooled patients visiting a tertiary healthcare center. An Osteoporotic Fractures in Men Study (MrOS) study conducted on elderly men found the prevalence of spondylolisthesis to be even higher at 31%³². However, this could be attributable to the differences in prevalence found across age groups^29,33 and gender³³. Nevertheless, the use of EOS in this study allowed accurate assessment of whole-body radiographic parameters to give the best analysis of risk factors associated with both conditions. Retrolisthesis, unlike spondylolisthesis, is less studied and its true value unknown⁴. This is the first, and largest study that uses EOS imaging to investigate the prevalence of retrolisthesis, which we found to be 17.1%. Contrary to an earlier study, this prevalence is higher and may again be attributed to differences in the studied populations³⁴.

Our study showed that spondylolisthesis and retrolisthesis are more prevalent in older ages, which may be attributed to its association with spinal degeneration³⁵. Unsurprisingly, higher ASA grades which are expected in the older age groups, are also found to be associated with spondylolisthesis³⁶. When age increases, the spine goes into progressive kyphosis with recruitment of compensatory mechanisms to keep itself balanced¹². The sudden increase in prevalence of spondylolisthesis in patients above 50 years old is likely reflective of exhausted physiological reserves, with acute worsening of the condition. This is supported by the concomitant findings of sagittal compensation such as increased PT (P < .001) and KAA (P = .011), and SCA (P = .007) in patients with spondylolisthesis^37,38 (Figure 1). The prevalence of retrolisthesis, on the other hand, is seen in all age groups and increases gradually with age, suggesting its possible compensatory role in sagittal balancing rather than being the primary pathology^39-42. Unlike spondylolisthesis which is often a pathological problem resulting from shear forces residing in the lordotic lumbar spine^43,44, as well as forward bending postures and activities⁴⁵, primary retrolisthesis is less common as minimal postures or activities drive the spine backwards. Increased TLA in patients with retrolisthesis are suggestive of adaptive changes following prolonged natural standing⁴¹ or sitting postures^40,41 where the patient employs posterior ligamentous complex to balance and conserve energy. This shifts the body’s centre of gravity backwards likely resulting in a backward shear force on the thoracolumbar and upper lumber vertebrae.

Females were found to have an increased prevalence of spondylolisthesis as compared to males. This may be due to the influence that hormones have on ligamentous laxity⁴⁶. This is analogous to female patients with adolescent idiopathic scoliosis, where ligamentous laxity has also been identified as a possible contributing factor⁴⁷. The association between lower limb pain with spondylolisthesis but not with lower back pain likely reflects the non-specificity of the latter symptom³¹, such that having a spondylolisthesis does not necessarily explain the cause of low back pain. However, lower limb pain which is often concordant with stenosis at the level of spondylolisthesis likely explains the symptoms and localises the pathology⁴⁶. This emphasizes the need to ascertain the true cause of low back pain even in the presence of a degenerative spondylolisthesis before instituting surgical treatment.

While it is possible that both spondylolisthesis and retrolisthesis vary somewhat in terms of aetiology, the result of vertebra translation should depend on the similar force principles. A forward-directed nett force should lead to spondylolisthesis and a backward-directed nett force retrolisthesis. Determinants of these forces include the posture and activities of the patient^40,48-50, which in turn influences the force magnitude on each lumbar vertebra. In our study, the higher prevalence of spondylolisthesis from L3/4 to L5/S1 levels and retrolisthesis from L1/2 to L3/4 further substantiates this point. Since lordosis occurs in the lumbar spine particularly the lower segments regardless of posture, and lower segments have a positive slope angle, under the pull of gravity, forward vertebral translation naturally ensues (Figure 2). Cranial to the apex of the lumbar curve, which usually resides in L3/4, an opposite force vector results in backward vertebral translation. Moreover, when sitting posture of the spine is considered, more forward force is generated (Figure 2). This has been shown in studies comparing standing and sitting postures^40,41,51,52 and explains the higher prevalence of spondylolisthesis in predominantly sitting occupations found in this study.

Figure 2.

Diagrammatic representation of the proposed mechanisms that results in spondylolisthesis.

In this study, PI is found to be higher in patients with spondylolisthesis as compared to those without (P<.001). This suggests that individual-specific pelvic morphology is a risk factor for this condition⁵³. In addition, increased PT was also found to be associated with spondylolisthesis. Although PT varies with posture^40,41,45 and its increase is likely contributed by spinopelvic compensation mentioned earlier^54,55, a paradoxic concomitant increase in SS, which should behave reciprocally, reinforces that this increase is likely to be also contributed by pelvic morphology. This can be further explained by the equation PI = PT + SS⁵⁶, where patients with a large PI naturally bears a larger PT and SS. Further findings of larger L₅I (P<.001), L₅T (P=.001) and L₅S (P=.015) associated with L4/5 spondylolisthesis substantiates this hypothesis. Failure to observe similar phenomenon in other intervertebral levels is likely due to the low prevalence of spondylolisthesis at those levels.

A larger L₄I and L₄S, being associated with spondylolisthesis (P=.003 and P=.045 respectively), is concordant with the existing literature which supports the association between slope angles and spondylolisthesis⁵⁷. The presence of retrolisthesis in association with a smaller L4S (P=.011), as well as a smaller SS (P=.033) is interesting and may be due to postural changes in sitting that stresses the spine in pelvic retroversion. From a clinical perspective, the authors hypothesize that tilt angles are more at risk of slippage in the more cranial vertebrae could be due to the rather horizontal sacral slope (Figure 3). On the contrary, slope angles appear important at L3/4 and L4/5 levels due to the proximity of vertebra to the gravity line⁴⁸. Only a trend towards SS predicting L5/S1 spondylolisthesis is observed could be related to the relative stiffness at the L5/S1 level in some patients due to transitional vertebra^58,59 and iliolumbar ligaments⁶⁰.

Figure 3.

Diagrammatic representation of how level-specific spinopelvic parameters LI, LT and LS may influence the occurrence of spondylolisthesis or retrolisthesis at common levels.

There are 3 limitations to this study. First, despite having a large sample size of 256 patients, this study was insufficiently powered to conclude if spondylolisthesis predisposes to cranial level retrolisthesis. This would be interesting since retrolisthesis can be a physiological phenomenon alone, or a compensatory mechanism for forward sagittal spinal imbalance⁴² where spondylolisthesis could have influenced the opposite translation of the cranial vertebrae. In order to resolve this, future larger scale studies with patients that have high grade spondylolisthesis and substantial forward imbalance can be performed. Second, the sole usage of standing lateral radiographs for identification of spondylolisthesis and retrolisthesis may not reflect the true behaviour of vertebral translation, which may vary with changes in spinal alignment. Flexion-extension stress radiographs or imaging in other postures, such as seating, may improve the detection of unstable spondylolisthesis and provide additional information useful for clinical decision making and surgical planning²⁰. In fact, as alignment changes from standing to sitting, the prevalence may change⁶¹. Nonetheless, we hypothesize that sitting occupations predisposes to spondylolisthesis but future large, powered studies are required to confirm this finding. Thirdly, in our cohort study, there were no high-grade spondylolisthesis. As low-grade spondylolisthesis is much more common, our study focuses on low-grade spondylolisthesis⁶².

In conclusion, this is the first study that documents the prevalence of spondylolisthesis and retrolisthesis simultaneously using the EOS technology, which is the gold standard radiological modality for the study of spinal and whole body alignment. It allows the further appreciation of both conditions, their mutual relationship, and associations with other clinical and radiological parameters. The information obtained incorporates the current state-of-art concepts in adult spinal deformity such as sagittal imbalance, compensatory mechanisms, and the potential clinical impact of postural variations. This study will continue to lay the platform for further studies of both conditions.

Footnotes

Acknowledgement

We thank Dr Lin Shuxun (Department of Orthopaedic Surgery, Ng Teng Fong General Hospital) for useful discussion and contributing to the manuscript.

Declaration of Conflicting Interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Ethical Approval

This study is approved by the local ethics board committee: NHG Domain Specific Review Board (DSRB): 2016/01 102.

ORCID iDs

Jun-HaoTan, MBBS (Sing), MRCS (Ire)

Tuan Hao Tan

Jiong Hao Jonathan Tan, MBBS (Sing), MRCS (Edin), MMED (Orth), FRCSEd (Orth)

References

Osterman

Schlenzka

Poussa

Seitsalo

Virta

. Isthmic spondylolisthesis in symptomatic and asymptomatic subjects, epidemiology, and natural history with special reference to disk abnormality and mode of treatment. Clin Orthop Relat Res. 1993;297:65-70.

Sengupta

Herkowitz

. Degenerative spondylolisthesis: review of current trends and controversies. Spine (Phila Pa 1976). 2005;30:S71-81. doi:10.1097/01.brs.0000155579.88537.8e

Jacobsen

Sonne-Holm

Rovsing

Monrad

Gebuhr

. Degenerative lumbar spondylolisthesis: an epidemiological perspective: the Copenhagen Osteoarthritis Study. Spine (Phila Pa 1976). 2007;32:120-125. doi:10.1097/01.brs.0000250979.12398.96

Berlemann

Jeszenszky

Bühler

Harms

. Mechanisms of retrolisthesis in the lower lumbar spine. A radiographic study. Acta Orthop Belg. 1999;65:472-477.

Vogt

Rubin

Palermo

, et al. Lumbar spine listhesis in older African American women. SPINE J. 2003;3:255-261. doi:10.1016/s1529-9430(03)00024-x

Shen

Razi

Lurie

Hanscom

Weinstein

. Retrolisthesis and lumbar disc herniation: a preoperative assessment of patient function. SPINE J. 2007;7:406-413. doi:10.1016/j.spinee.2006.08.011

Iguchi

Wakami

Kurihara

Kasahara

Yoshiya

Nishida

. Lumbar multilevel degenerative spondylolisthesis: radiological evaluation and factors related to anterolisthesis and retrolisthesis. J Spinal Disord Tech. 2002;15:93-99. doi:10.1097/00024720-200204000-00001

Kim

Bridwell

Lenke

Rhim

Cheh

. An analysis of sagittal spinal alignment following long adult lumbar instrumentation and fusion to L5 or S1: can we predict ideal lumbar lordosis? Spine (Phila Pa 1976). 2006;31:2343-2352. doi:10.1097/01.brs.0000238970.67552.f5

Lafage

Schwab

Patel

Hawkinson

Farcy

. Pelvic tilt and truncal inclination: two key radiographic parameters in the setting of adults with spinal deformity. Spine (Phila Pa 1976). 2009;34:E599-606. doi:10.1097/BRS.0b013e3181aad219

10.

Hey

HWD

Tan

Ong

Kumar

Liu

Wong

. Pelvic and sacral morphology and their correlation with pelvic incidence, lumbar lordosis, and lumbar alignment changes between standing and sitting postures. Clin Neurol Neurosurg. 2021;211:107019. doi:10.1016/j.clineuro.2021.107019

11.

Pitkänen

Manninen

Lindgren

Sihvonen

Airaksinen

Soimakallio

. Segmental lumbar spine instability at flexion-extension radiography can be predicted by conventional radiography. Clin Radiol. 2002;57:632-639. doi:10.1053/crad.2001.0899

12.

Barrey

Roussouly

Le Huec

D'Acunzi

Perrin

. Compensatory mechanisms contributing to keep the sagittal balance of the spine. Eur Spine J. 2013;22:S834-841.

13.

Husson

Mallet

Parent

, et al. The lumbar-pelvic-femoral complex: applications in spinal imbalance. Orthop Traumatol Surg Res. 2010;96:S1-S9.

14.

Glaser

Doan

Newton

. Newton Comparison of 3-dimensional spinal reconstruction accuracy: biplanar radiographs with EOS versus computed tomography. Spine (Phila Pa 1976). 2012;37:1391-1397. doi:10.1097/BRS.0b013e3182518a15

15.

Somoskeöy

Tunyogi-Csapó

Bogyó

Illés

. Accuracy and reliability of coronal and sagittal spinal curvature data based on patient-specific three-dimensional models created by the EOS 2D/3D imaging system. Spine J. 2012;12:1052-1059. doi:10.1016/j.spinee.2012.10.002

16.

EOS Imaging. https://www.eos-imaging.com/ Accessed 20/2/2020, 2020.

17.

Hey

HWD

Tan

Thadani

Liu

Wong

. Characterisation of Sagittal Spine Alignment With Reference to the Gravity Line and Vertebral Slopes - An Analysis of Different Roussouly Curves. Spine (Phila Pa 1976). 2020;45(9):E481-E488. doi:10.1097/BRS.0000000000003379

18.

Riihimaki

. Low-back pain, its origin and risk indicators. Scand J Work Environ Health. 1991;17:81-90.

19.

Atlas

Deyo

. Evaluating and managing acute low back pain in the primary care setting. J Gen Intern Med. 2001;16:120-131. doi:10.1111/j.1525-1497.2001.91141.x

20.

Hey

Lau

Lim

, et al. Slump sitting X-ray of the lumbar spine is superior to the conventional flexion view in assessing lumbar spine instability. Spine J. 2017;17:360-368. doi:10.1016/j.spinee.2016.10.003

21.

Ferreiro Perez

Garcia Isidro

Ayerbe

Castedo

Jinkins

. Evaluation of intervertebral disc herniation and hypermobile intersegmental instability in symptomatic adult patients undergoing recumbent and upright MRI of the cervical or lumbosacral spines. Eur J Radiol. 2007;62:444-448. doi:10.1016/j.ejrad.2006.12.007

22.

O'Sullivan

. Lumbar segmental ‘instability': clinical presentation and specific stabilizing exercise management. Man Ther. 2000;5:2-12. doi:10.1054/math.1999.0213

23.

Wollowick

Sarwahi

. Spondylolisthesis: Diagnosis, Non-Surgical Management, and Surgical Techniques. 2015th ed. United State: Springer.

24.

Huang

Bohlman

Thompson

Poe-Kochert

. Predictive value of pelvic incidence in progression of spondylolisthesis. Spine (Phila Pa 1976). 2003;28:2381-2385. doi:10.1097/01.BRS.0000085325.42542.38

25.

Passias

Poorman

Yang

, et al. Surgical Treatment Strategies for High-Grade Spondylolisthesis: A Systematic Review. Int J Spine Surg. 2015;9:50. doi:10.14444/2050

26.

Fischgrund

Mackay

Herkowitz

Brower

Montgomery

Kurz

. Volvo Award Winner in Clinical Studies: Degenerative Lumbar Spondylolisthesis With Spinal Stenosis: A Prospective, Randomized Study Comparing Decompressive Laminectomy and Arthrodesis With and Without Spinal Instrumentation. Spine (Phila Pa 1976). 1997;22:2807-2812. doi:10.1097/00007632-199712150-00003

27.

DiPaola

Molinari

. Posterior lumbar interbody fusion. J Am Acad Orthop Surg. 2008;16:130-139. doi:10.5435/00124635-200803000-00004

28.

Weinstein

Lurie

Tosteson

, et al. Surgical compared with nonoperative treatment for lumbar degenerative spondylolisthesis. four-year results in the Spine Patient Outcomes Research Trial (SPORT) randomized and observational cohorts. J Bone Joint Surg Am. 2009;91:1295-1304. doi:10.5435/10.2106/JBJS.H.00913

29.

Virta

Rönnemaa

Osterman

Aalto

Laakso

. Prevalence of isthmic lumbar spondylolisthesis in middle-aged subjects from eastern and western Finland. J Clin Epidemiol. 1992;45:917-922. doi:10.1016/0895-4356(92)90075-x

30.

Horikawa

Kasai

Yamakawa

Sudo

Uchida

. Prevalence of osteoarthritis, osteoporotic vertebral fractures, and spondylolisthesis among the elderly in a Japanese village. J Orthop Surg (Hong Kong). 2006;14:9-12. doi:10.1177/230949900601400103

31.

Kalichman

Kim

Guermazi

Berkin

Hunter

. Spondylolysis and spondylolisthesis: prevalence and association with low back pain in the adult community-based population. Spine (Phila Pa 1976). 2009;34 199-205. doi:10.1097/BRS.0b013e31818edcfd

32.

Denard

Holton

Miller

, et al. Lumbar spondylolisthesis among elderly men: prevalence, correlates, and progression. Spine (Phila Pa 1976). 2010;35:1072-1078. doi:10.1097/BRS.0b013e3181bd9e19

33.

Vogt

Rubin

Valentin

, et al. Lumbar olisthesis and lower back symptoms in elderly white women. The Study of Osteoporotic Fractures. Spine (Phila Pa 1976). 1998;23:2640-2647. doi:10.1097/00007632-199812010-00020

34.

Wang

Gong

, et al. Prevalence and risk factors of lumbar spondylolisthesis in elderly Chinese men and women. Eur Radiol. 2014;24:441-448. doi:10.1007/s00330-013-3041-5

35.

Benoist

. Natural history of the aging spine. Eur Spine J. 2003;12 S86-89. doi:10.1007/s00586-003-0593-0

36.

Kilinçer

Steinmetz

Sohn

Benzel

Bingaman

. Effects of age on the perioperative characteristics and short-term outcome of posterior lumbar fusion surgery. J Neurosurg Spine. 2005;3:34-39. 10.3171/spi.2005.3.1.0034

37.

Hey

HWD

Tan

Chin

Liu

Wong

. Comparison of whole body sagittal alignment during directed vs natural, relaxed standing postures in young, healthy adults. Spine J. 2019;19(11):1832-1839. 10.1016/j.spinee.2019.06.017

38.

Hey

HWD

Lin

Tay

Liu

Wong

. Understanding "Kyphosis" and "Lordosis" for Sagittal Balancing in Two Common Standing Postures. Spine (Phila Pa 1976). 2021;46(23):1603-1611. doi:10.1097/brs.0000000000004106

39.

Jeon

Park

Chung

Son

Lee

Kim

. Degenerative retrolisthesis: is it a compensatory mechanism for sagittal imbalance? Bone Joint J. 2013;95-B(9):1244-1249. doi:10.1302/0301-620X.95B9.31237

40.

Hey

HWD

Teo

AQA

Tan

, et al. How the spine differs in standing and in sitting-important considerations for correction of spinal deformity. Spine J. 2017;17:799-806. doi:10.1016/j.spinee.2016.03.056

41.

Hey

Wong

Lau

, et al. Differences in erect sitting and natural sitting spinal alignment-insights into a new paradigm and implications in deformity correction. Spine J. 2017;17:183-189. doi:10.1016/j.spinee.2016.08.026

42.

Jeon

Kim

. Retrolisthesis as a compensatory mechanism in degenerative lumbar spine. J Korean Neurosurg Soc. 2015;57(3):78-84. doi:10.3340/jkns.2015.57.3.178

43.

Motley

Nyland

Jacobs

Caborn

. The pars interarticularis stress reaction, spondylolysis, and spondylolisthesis progression. J Athl Train. 1998;33:351-358.

44.

Konz

Goel

Grobler

, et al. The pathomechanism of spondylolytic spondylolisthesis in immature primate lumbar spines in vitro and finite element assessments. Spine (Phila Pa 1976). 2001;26:E38-49. doi:10.1097/00007632-200102150-00003

45.

Hey

HWD

Lau

Tan

, et al. Lumbar Spine Alignment in Six Common Postures: An ROM Analysis With Implications for Deformity Correction. Spine (Phila Pa 1976). 2017;42:1447-1455. 10.1097/BRS.0000000000002131

46.

Nadaud

McClure

Weiner

. Do facet joint capsular ligaments contain estrogen receptors? Application to pathogenesis of degenerative spondylolisthesis. Am J Orthop (Belle Mead NJ). 2001;30(10):753-754.

47.

Bagnall

Al Hamsi

Al Kaabi

D’souza

. Incidence of ligamentous laxity and scoliosis among the population of the United Arab Emirates. Scoliosis. 2012;7:O70-O70. doi:10.1186/1748-7161-7-S1-O70

48.

Hey

HWD

Tan

Kantharajanna

, et al. Using spinopelvic parameters to estimate residual lumbar lordosis assuming previous lumbosacral fusion-a study of normative values. Spine J. 2018;18(13):422-429. doi:10.1016/j.spinee.2017.08.232

49.

Hey

HWD

Loh

KYS

, et al. Sagittal Radiographic Parameters of the Spine in Three Physiological Postures Characterized Using a Slot Scanner and Their Potential Implications on Spinal Weight-Bearing Properties. Asian Spine J. 2021;15(1):23-31. 10.31616/asj.2019.0198

50.

Hey

HWD

Tan

KLM

Lau

JWP

Liu

Wong

. The Impact of Radiographic Lower Limb-Spinal Length Proportion on Whole-Body Sagittal Alignment. Spine (Phila Pa 1976). 2022;47(1):E38-e45. doi:10.1097/BRS.0000000000004240

51.

Hey

HWD

Ramos

MRD

Lau

, et al. Risk Factors Predicting C- Versus S-shaped Sagittal Spine Profiles in Natural, Relaxed Sitting: An Important Aspect in Spinal Realignment Surgery. Spine (Phila Pa 1976). 2020;45(24):1704-1712. doi:10.1097/BRS.0000000000003670

52.

Hey

HWD

Lim

JCL

Law

Liu

Wong

. Understanding the Pathophysiology of L5-S1 Loss of Lordosis and Retrolisthesis: An EOS Study of Lumbopelvic Movement Between Standing and Slump Sitting Postures. World Neurosurg. 2021. doi:10.1016/j.wneu.2021.11.034

53.

Tebet

. Current concepts on the sagittal balance and classification of spondylolysis and spondylolisthesis. Rev Bras Ortop. 2014;49:3-12. doi:10.1016/j.rboe.2014.02.003

54.

Roussouly

Pinheiro-Franco

. Biomechanical analysis of the spino-pelvic organization and adaptation in pathology. Eur Spine J. 2011;20:609-618. doi:10.1007/s00586-011-1928-x

55.

La Maida

Zottarelli

Mineo

Misaggi

. Sagittal balance in adolescent idiopathic scoliosis: radiographic study of spino-pelvic compensation after surgery. Eur Spine J. 2013;22:S859-867. doi:10.1007/s00586-013-3018-8

56.

Le Huec

Aunoble

Philippe

Nicolas

. Pelvic parameters: origin and significance. Eur Spine J. 2011;20:564-571. doi:10.1007/s00586-011-1940-1

57.

Marty

Boisaubert

Descamps

, et al. The sagittal anatomy of the sacrum among young adults, infants, and spondylolisthesis patients. Eur Spine J. 2002;11:119-125. doi:10.1007/s00586-001-0349-7

58.

Viner

Lee

Adams

. Posteroanterior Stiffness in the Lumbosacral Spine: The Correlation Between Adjacent Vertebral Levels. Spine (Phila Pa 1976). 1997;22:2724-2729. doi:10.1097/00007632-199712010-00004

59.

Mahato

. Facet dimensions, orientation, and symmetry at L5-S1 junction in lumbosacral transitional States. Spine (Phila Pa 1976). 2011;36:E569-573. doi:10.1097/BRS.0b013e3181f6ecb2

60.

Pool-Goudzwaard

Hoek van Dijke

Mulder

Spoor

Snijders

Stoeckart

. The iliolumbar ligament: its influence on stability of the sacroiliac joint. Clin Biomech (Bristol, Avon). 2003;18:99-105. doi:10.1016/s0268-0033(02)00179-1

61.

Vaccaro

A.R.

Ring

Scuderi

Cohen

Garfin

. Predictors of Outcome in Patients With Chronic Back Pain and Low-Grade Spondylolisthesis. Spine 1997. 22(17):2030-2034. doi:10.1097/00007632-199709010-00018

62.

Cho

Park

Kim

Jung

Lee

. The Effect of Standing and Different Sitting Positions on Lumbar Lordosis: Radiographic Study of 30 Healthy Volunteers. Asian Spine J 2015;9(5):762-769. doi:10.4184/asj.2015.9.5.762