How does sagittal spinopelvic alignment of lumbar multisegmental spondylolysis differ from monosegmental spondylolysis?

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  • 1 Department of Spine Surgery, Drum Tower Hospital, Clinical College of Nanjing Medical University, Nanjing; and
  • | 2 Department of Spine Surgery, Drum Tower Hospital, Medical School of Nanjing University, Nanjing, China
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OBJECTIVE

The aim of this study was to investigate sagittal alignment and compensatory mechanisms in patients with monosegmental spondylolysis (mono_lysis) and multisegmental spondylolysis (multi_lysis).

METHODS

A total of 453 adult patients treated for symptomatic low-grade spondylolytic spondylolisthesis were retrospectively studied at a single center. Patients were divided into 2 subgroups, the mono_lysis group and the multi_lysis group, based on the number of spondylolysis segments. A total of 158 asymptomatic healthy volunteers were enrolled in this study as the control group. Radiographic parameters measured on standing sagittal radiographs and the ratios of L4–S1 segmental lordosis (SL) to lumbar lordosis (L4–S1 SL/LL) and pelvic tilt to pelvic incidence (PT/PI) were compared between all experimental groups.

RESULTS

There were 51 patients (11.3%) with a diagnosis of multi_lysis in the spondylolysis group. When compared with the control group, the spondylolysis group exhibited larger PI (p < 0.001), PT (p < 0.001), LL (p < 0.001), and L4–S1 SL (p = 0.025) and a smaller L4–S1 SL/LL ratio (p < 0.001). When analyzing the specific spondylolysis subgroups, there were no significant differences in PI, but the multi_lysis group had a higher L5 incidence (p = 0.004), PT (p = 0.018), and PT/PI ratio (p = 0.039). The multi_lysis group also had a smaller L4–S1 SL/LL ratio (p = 0.012) and greater sagittal vertical axis (p < 0.001).

CONCLUSIONS

A high-PI spinopelvic pattern was involved in the development of spondylolytic spondylolisthesis, and a larger L5 incidence might be associated with the occurrence of consecutive multi_lysis. Unlike patients with mono_lysis, individuals with multi_lysis were characterized by an anterior trunk, insufficiency of L4–S1 SL, and pelvic retroversion.

ABBREVIATIONS

LDI = lordosis distribution index; LL = lumbar lordosis; L5I = L5 incidence; mono_lysis = monosegmental spondylolysis; multi_lysis = multisegmental spondylolysis; ODI = Oswestry Disability Index; PI = pelvic incidence; PT = pelvic tilt; QOL = quality of life; SA = slip angle; SL = segmental lordosis; SP = slip percentage; SS = sacral slope; SVA = sagittal vertical axis; TK = thoracic kyphosis; VAS = visual analog scale.

OBJECTIVE

The aim of this study was to investigate sagittal alignment and compensatory mechanisms in patients with monosegmental spondylolysis (mono_lysis) and multisegmental spondylolysis (multi_lysis).

METHODS

A total of 453 adult patients treated for symptomatic low-grade spondylolytic spondylolisthesis were retrospectively studied at a single center. Patients were divided into 2 subgroups, the mono_lysis group and the multi_lysis group, based on the number of spondylolysis segments. A total of 158 asymptomatic healthy volunteers were enrolled in this study as the control group. Radiographic parameters measured on standing sagittal radiographs and the ratios of L4–S1 segmental lordosis (SL) to lumbar lordosis (L4–S1 SL/LL) and pelvic tilt to pelvic incidence (PT/PI) were compared between all experimental groups.

RESULTS

There were 51 patients (11.3%) with a diagnosis of multi_lysis in the spondylolysis group. When compared with the control group, the spondylolysis group exhibited larger PI (p < 0.001), PT (p < 0.001), LL (p < 0.001), and L4–S1 SL (p = 0.025) and a smaller L4–S1 SL/LL ratio (p < 0.001). When analyzing the specific spondylolysis subgroups, there were no significant differences in PI, but the multi_lysis group had a higher L5 incidence (p = 0.004), PT (p = 0.018), and PT/PI ratio (p = 0.039). The multi_lysis group also had a smaller L4–S1 SL/LL ratio (p = 0.012) and greater sagittal vertical axis (p < 0.001).

CONCLUSIONS

A high-PI spinopelvic pattern was involved in the development of spondylolytic spondylolisthesis, and a larger L5 incidence might be associated with the occurrence of consecutive multi_lysis. Unlike patients with mono_lysis, individuals with multi_lysis were characterized by an anterior trunk, insufficiency of L4–S1 SL, and pelvic retroversion.

ABBREVIATIONS

LDI = lordosis distribution index; LL = lumbar lordosis; L5I = L5 incidence; mono_lysis = monosegmental spondylolysis; multi_lysis = multisegmental spondylolysis; ODI = Oswestry Disability Index; PI = pelvic incidence; PT = pelvic tilt; QOL = quality of life; SA = slip angle; SL = segmental lordosis; SP = slip percentage; SS = sacral slope; SVA = sagittal vertical axis; TK = thoracic kyphosis; VAS = visual analog scale.

Lumbar spondylolysis, sometimes combined with spondylolisthesis, predominantly occurs at the lumbosacral monosegment (mono_lysis).1,2 It is rare but possible for spondylolysis to be detected at consecutive multiple regions of the lumbar spine (multi_lysis).3,4 Spondylolysis, with or without spondylolisthesis, is usually asymptomatic; however, some patients may present with intractable back pain or radicular symptoms.2 If conservative treatment fails, surgical intervention is an effective solution to achieve solid fusion, neurological decompression, and restoration of lumbar alignment.5

The pathological mechanisms behind lumbar spondylolysis are still not fully understood. Spinopelvic alignment is an important factor in the occurrence and progression of single-level spondylolytic spondylolisthesis.6,7 Studies have reported that L5–S1 spondylolytic spondylolisthesis is associated with increased pelvic incidence (PI) compared with that observed in a normal population.7,8 As demonstrated in biomechanical studies, increased PI generates higher repetitive stress at the pars interarticularis and subsequently results in the development of lumbosacral spondylolysis.9 The status of the sagittal plane, such as insufficient lordosis, pelvic retroversion, and anterior sagittal malalignment, has been reported to be associated with clinical presentation.10 Analyses of sagittal spinopelvic alignment in patients with lumbosacral spondylolytic spondylolisthesis have led to the development of surgical algorithms and assessment of treatment outcomes.11,12 Inadequate restoration of lumbar alignment is reported to be related to poor patient-reported outcomes,11,13 mechanical complications,12,13 and adjacent-segment disease.14,15

Lumbosacral consecutive multi_lysis often requires surgical intervention because of potential segmental instability. However, to our knowledge, no studies have analyzed the spinopelvic alignment of multi_lysis, whereas only sporadic case reports in the literature have mentioned or described such a rare disease.4,16,17 Comprehensive interpretation of the sagittal alignment pattern and compensatory mechanisms of sagittal balance are essential for surgical intervention to correct multi_lysis. The goals of this study were to 1) investigate the pattern of sagittal alignment in spondylolytic spondylolisthesis patients (both mono_lysis and multi_lysis) in comparison with healthy individuals and 2) illustrate differences of sagittal alignment and compensatory mechanisms in patients diagnosed with mono_lysis versus multi_lysis.

Methods

Patient Population

Patients diagnosed with symptomatic spondylolysis with spondylolisthesis who previously underwent surgical intervention at our center between January 2007 and January 2018 were retrospectively studied. Enrolled patients had to meet the following inclusion criteria: 1) age 18 years or older and 2) symptomatic lumbar spondylolysis with at least 1 level of spondylolisthesis (Meyerding’s grade I or II). Exclusion criteria preventing a patient from being studied included 1) diagnosis of degenerative spondylolisthesis; 2) exhibition of lumbar scoliosis > 10°; and 3) a previous history of spinal surgery, trauma, infection, or fracture of the pelvis or lower limbs. All spondylolysis patients were diagnosed by 3D-CT radiography of the lumbar spine. Spondylolisthesis was defined as a forward slip of one vertebral body by at least 5% in relation to the next most caudal vertebral body on upright neutral lateral radiography.18 Patient demographic data, including age, sex, BMI, and work status, were recorded. The enrolled patients with spondylolysis were divided into 2 subgroups: the mono_lysis subgroup and the multi_lysis subgroup (Fig. 1). The mono_lysis group included patients with monosegmental spondylolytic spondylolisthesis, whereas the multi_lysis group included patients with multilevel spondylolysis and spondylolisthesis in at least one of the spondylolytic levels. A cohort of healthy adult volunteers from the Chinese Han population were recruited into the control group. All studies were approved by the institutional review board committee.

FIG. 1.
FIG. 1.

Representative lateral radiographs obtained in a patient with double-level spondylolysis (A), a patient with mono_lysis (B), and a healthy individual (C). A: A 59-year-old female with L4–5 and L5–S1 double-level spondylolysis. PI = 70.6°, PT/PI ratio = 42%, L5I = 57.0°, LL = 45.20°, LDI = 16%, SVA = 92 mm. B: A 52-year-old female with L5–S1 mono_lysis. PI = 56.1°, PT/PI ratio = 30.4%, L5I = 25.7°, LL = 57.4°, LDI = 63%, SVA = 9 mm. C: A 46-year-old healthy individual without back pain. PI = 44.3°, PT/PI ratio = 16%, L5I = 14.1°, LL = 52°, LDI = 74%, SVA = −12 mm.

Radiography Analyses

Radiographic parameters were measured by 2 senior spinal surgeons using upright radiographs, and the mean values were adapted for the analyses (Fig. 2).7,11,19 Slip percentage (SP) and slip angle (SA) of the L3–4, L4–5, and L5–S1 levels were measured at the spondylolysis and spondylolisthesis levels, respectively. Pelvic parameters, including PI, pelvic tilt (PT), and sacral slope (SS), were measured as previously described.20 The PT/PI ratio was computed to investigate pelvic retroversion.21,22 Also, pelvic balance was determined on the nomogram of PT and SS measurements, as described by Hresko et al.23 L5 incidence (L5I) was measured from the middle of the femoral heads to the middle of the sacrum plateau and a line perpendicular to the upper endplate of L5.24 Lumbar lordosis (LL) was measured from the upper endplate of the L1 vertebra to the upper endplate of S1. L4–S1 segmental lordosis (SL) was measured from the upper endplate of L4 to the upper endplate of S1. The lordosis distribution index (LDI) was defined as the ratio of L4–S1 SL to LL, allowing greater understanding of lordosis distribution as upper- and lower-arc lordoses.12,13 Thoracic kyphosis (TK) was measured from the upper endplate of T5 to the lower endplate of the T12 vertebra. Global sagittal alignment was assessed by the sagittal vertical axis (SVA; the distance between a plumb line from the center of the C7 vertebral body and posterior superior corner of S1). An unbalanced alignment was characterized by an SVA ≥ 4 cm, following the Scoliosis Research Society–Schwab adult spinal deformity classification.25

FIG. 2.
FIG. 2.

Radiological parameters measured on upright radiographs. A: Pelvic parameters: PI, PT, SS, and L5I. B: Slip parameters: slip angle (α), slip percentage (line bc/line ac × 100%). C: Sagittal alignment parameters: L4–S1 segmental lordosis (L4–S1 SL), LL, TK, and SVA.

Quality of Life

Preoperative quality-of-life (QOL) questionnaires were administered to patients. The Oswestry Disability Index (ODI) and visual analog scale (VAS) for leg pain and back pain were used to evaluate the QOL.

Statistical Analysis

Statistical analyses were performed using IBM SPSS (version 20.0, IBM Corp.). The mean and standard deviation were calculated for continuous variables. The independent-samples t-test was performed to evaluate the differences between 2 groups. Differences among 3 groups were evaluated using one-way ANOVA and chi-square tests. We first performed an analysis of the demographic data for each experimental group. Next, comparison analysis of the data obtained from radiological analysis was performed between the control and the spondylolysis groups, and among the control, multi_lysis, and mono_lysis groups. Pearson correlations were also performed for the multi_lysis group. Lastly, QOL scores were compared between the spondylolysis subgroups. A p value < 0.05 was considered as statistically significant.

Results

Patient Demographics

A total of 158 healthy volunteers and 453 spondylolysis patients were included in this study (Table 1). In the spondylolysis group, 51 patients (11.3%) were found to have multiple spondylolysis and were categorized into the multi_lysis group. There were no significant differences observed regarding age, sex, BMI, or work status among the 3 groups.

TABLE 1.

Demographic data among the normal group and the 2 spondylolysis subgroups

Control GroupMulti_Lysis GroupMono_Lysis Groupp Value
Mean age, yrs47.1 ± 11.350.1 ± 10.448.0 ± 13.20.327
Mean BMI23.1 ± 3.724.4 ± 5.823.6 ± 4.30.153
Male/female62/9615/36143/2590.425
Work status
 Full or part time7822218
 Retired34151020.154
 Other461482

Values are presented as the number of patients unless otherwise indicated. Mean values are presented as the mean ± SD.

Spondylolisthesis Parameters

Spondylolytic spondylolisthesis was observed at L5–S1 in 295 patients, at L4–5 in 102 patients, and at L3–4 in 5 patients in the mono_lysis group. The most common pathology observed in the multi_lysis group was L4–5 and L5–S1 double-level spondylolysis in 40 patients (78.4%), followed by L3–4 and L4–5 2-level spondylolysis in 6 patients (11.8%) and L3–4, L4–5, and L5–S1 3-level spondylolysis in 5 patients (9.8%). Spondylolisthesis was detected at a single level in 17 patients (L4–5 in 9 and L5–S1 in 8), at 2 levels in 32 patients (L4–5 and L5–S1 in 29 and L3–4 and L4–5 in 3), and at 3 levels (L3–4, L4–5, and L5–S1) in 2 patients in the multi_lysis group.

Spondylolisthesis-related parameters are summarized in Table 2. Both SP and SA at the L3–4 and L4–5 levels were found to be similar between the multi_lysis and mono_lysis groups, but were significantly lower at the L5–S1 level in the multi_lysis group (p = 0.002 and p < 0.001, respectively).

TABLE 2.

Comparison of mean slipping parameters between the spondylolysis subgroups

Multi_Lysis GroupMono_Lysis Groupp Value
L3–4 SP (%)10.0 ± 3.510.0 ± 3.60.202
L4–5 SP (%)23.5 ± 11.023.3 ± 10.00.915
L5–S1 SP (%)17.9 ± 10.523.5 ± 10.40.002
L3–4 SA (°)12.9 ± 2.56.7 ± 6.50.126
L4–5 SA (°)8.8 ± 7.86.9 ± 5.90.125
L5–S1 SA (°)7.0 ± 9.89.9 ± 6.6<0.001

Sagittal Alignment Assessment

Compared with the control group, the spondylolysis group exhibited significantly larger PI (p < 0.001), PT (p < 0.001), SS (p < 0.001), PT/PI ratio (p < 0.001), and L5I (p < 0.001) (Fig. 3). Although a significantly higher LL (p < 0.001) and slightly higher L4–S1 LL (p = 0.025) were detected in the spondylolysis group, the SVA (p = 0.003) was positive in comparison with the control group due to significant decreases in TK (p < 0.001) and LDI (p < 0.001).

FIG. 3.
FIG. 3.

Comparison of sagittal alignment parameters between the control group and the spondylolysis group.

Sagittal alignment parameter data analyzed by one-way ANOVA among the control, multi_lysis, and mono_lysis groups are shown in Table 3. PI and SS were found to be similar in the multi_lysis and mono_lysis groups. However, a slightly greater PT (18.9° ± 9.0° vs 16.3° ± 7.6°, p = 0.018) and PT/PI (32% ± 12% vs 29% ± 10%, p = 0.039) were observed in the multi_lysis group. In addition, L5I was significantly greater in the multi_lysis group than in the mono_lysis group (30.8° ± 14.8° vs 26.0° ± 11.2°, p = 0.004). Remarkably, smaller LL (53.4° ± 12.0° vs 57.6° ± 10.7°, p = 0.005), L4–S1 SL (32.8° ± 13.2° vs 37.2° ± 9.1°, p = 0.004), and LDI (59% ± 21% vs 64% ± 12%, p = 0.012) were observed in the multi_lysis versus the mono_lysis group. There were no significant differences in TK observed between the subgroups.

TABLE 3.

Comparison of mean sagittal parameters among the control, multi_lysis, and mono_lysis groups

p Value
ControlMulti_LysisMono_Lysis1-Way ANOVAMulti_Lysis vs ControlMono_Lysis vs ControlMulti_Lysis vs Mono_Lysis
PI (°)46.2 ± 10.158.0 ± 11.955.9 ± 11.3<0.001<0.001<0.0010.206
PT (°)11.2 ± 6.219.0 ± 9.016.3 ± 7.6<0.001<0.001<0.0010.018
SS (°)34.9 ± 7.639.1 ± 8.739.6 ± 8.3<0.0010.001<0.0010.679
L5I (°)18.2 ± 9.430.8 ± 14.826.0 ± 11.2<0.001<0.001<0.0010.004
LL (°)50.5 ± 9.953.4 ± 12.057.6 ± 10.7<0.0010.084<0.0010.005
L4–S1 SL (°)34.8 ± 7.732.8 ± 13.237.2 ± 9.1<0.0010.1860.0040.004
TK (°)37.2 ± 11.926.0 ± 11.128.0 ± 9.2<0.001<0.001<0.0010.157
SVA (mm)−5.3 ± 24.924.0 ± 39.71.8 ± 35.7<0.001<0.0010.021<0.001
PT/PI (%)23 ± 1132 ± 1229 ± 10<0.001<0.001<0.0010.039
LDI (%)69 ± 1359 ± 2164 ± 12<0.001<0.001<0.0010.012

As shown in Table 3, the multi_lysis group had a significantly greater SVA than the mono_lysis group (24.0 ± 39.7 mm vs 1.87 ± 35.7 mm, p < 0.001). When compared with the mono_lysis group, more patients in the multi_lysis group were shown to have an SVA ≥ 4 cm (29.4% vs 13.7%, p = 0.003) and an unbalanced pelvis with high PT/low SS (54.9% vs 40.8%, p = 0.039; Table 4).

TABLE 4.

Comparison of spinal and pelvic balance between the multi_lysis group and the mono_lysis group

Multi_LysisMono_Lysisp Value
Spinal balance, cm
 SVA ≥41555
 SVA <4363470.003
Pelvic balance
 Low PT/high SS232380.039
 High PT/low SS28164

Values are presented as the number of patients unless otherwise indicated.

In the multi_lysis group, PI was positively correlated with PT (r = 0.668, p < 0.001), SS (r = 0.641, p < 0.001), L5I (r = 0.745, p < 0.001), LL (r = 0.337, p = 0.016), and PT/PI ratio (r = 0.358, p = 0.010). In the same group, PI was negatively correlated with LDI (r = −0.426, p = 0.002) (Table 5). There were also positive correlations between L5I and PT (r = 0.860, p < 0.001), PT/PI ratio (r = 0.707, p < 0.001), and SVA (r = 0.356, p = 0.010). However, L5I was shown to negatively correlate with TK (r = −0.327, p = 0.019), L4–S1 SL (r = −0.548, p < 0.001), and LDI (r = −0.724, p < 0.001).

TABLE 5.

Pearson correlations in the multi_lysis group

PIL5I
Rp ValueRp Value
PT (°)0.668<0.0010.860<0.001
SS (°)0.641<0.0010.1650.247
L5I (°)0.745<0.0010.745<0.001
LL (°)0.3370.016−0.1070.454
L4–S1 SL (°)−0.0970.5−0.548<0.001
TK (°)−0.2410.089−0.3270.019
SVA (mm)0.2470.080.3560.01
PT/PI (%)0.3580.010.707<0.001
LDI (%)−0.4260.002−0.724<0.001

Quality of Life

Regarding both functional and clinical outcomes, the multi_lysis group reported worse ODI scores (mean 55.7 ± 10.1 vs 44.1 ± 11.4, p < 0.001) and VAS back pain scores (mean 6.6 ± 2.0 vs 6.0 ± 1.6, p = 0.016) than the mono_lysis group. No significant differences in VAS leg pain scores were observed when comparing the 2 subgroups.

Discussion

The goal of this study was to illustrate the sagittal alignment pattern in a large cohort of patients diagnosed with spondylolytic spondylolisthesis, including both multi_lysis and mono_lysis. We observed that patients with multi_lysis or mono_lysis exhibited abnormal pelvic morphology and orientation, insufficient LL, and forward trunk in comparison with healthy controls. It is worth mentioning that patients in the multi_lysis group had a significantly higher PT and PT/PI ratio and lower LL, L4–S1 SL, and LDI, which results in an increased tendency for sagittal decompensation. At the same time, L5I was detected to be significantly elevated in the multi_lysis group and significantly correlated with PT, PT/PI, SVA, L4–S1 SL, and LDI. In addition, the multi_lysis group had slightly worse ODI scores and VAS back pain scores than the mono_lysis group.

In this study, there was an 11.3% incidence of multi_lysis in patients with spondylolytic spondylolisthesis. Ravichandran26 reported that 1.48% of patients with back pain have multi_lysis. However, in a study of Japanese general individuals by Sakai et al.,4 the incidence of multi_lysis was 0.3% (5 of 2000). One reason for this inconsistency may be because our study is based on a cohort of patients diagnosed with spondylolytic spondylolisthesis who previously underwent surgical intervention.

PI, which is strongly correlated with PT and other sagittal alignment parameters, is one of the most important anatomical parameters in the sagittal plane. As demonstrated in biomechanical studies, PI may be associated with the development of spondylolysis as well as the progression of spondylolisthesis.7,9 PI was once thought to be greater in patients with multiple spondylolysis. In a study including only 5 patients diagnosed with double-level spondylolysis, PI was found to be higher in double-level spondylolysis versus single-level spondylolysis (61.0° ± 10.8° vs 71.0° ± 7.7°, p = 0.037). Nevertheless, based on a large cohort of spondylolysis patients, our study found no statistically significant differences in PT when comparing the multi_lysis and mono_lysis groups (58.0° ± 11.9° vs 55.9° ± 11.3°, p = 0.206). One explanation for this inconsistency may be due to the fact that the occurrence of spondylolysis in some patients (8 of 51 multi_lysis patients with PI < 45°) might result from the “nutcracker” mechanism.6,7 In addition, both Oh et al.19 and Park et al.27 found that the PI parameter did not statistically differ between the L4–5 mono_lysis and L5–S1 mono_lysis groups. Here, we assumed that multi_lysis was an accidental event for more than single spondylolytic segments occurring in a single patient, who had a shear stress impact on multisegmental posterior element dysplasia and/or a weak muscle-ligament-iliac complex.7,9,28

This study demonstrated that increased PI in multi_lysis cases was correlated with increased L5I (r = 0.745, p < 0.001). Similar to PI, L5I represents the orientation of the L5 vertebra and regulates the mechanical environment of the lower lumbar spine. Previously, Zhu et al.24 demonstrated that strong correlations exist between L5I and PI or sagittal alignment parameters in healthy individuals (r = 0.818, p < 0.001), indicating that L5I is a crucial parameter for the lumbosacral region. Nevertheless, it was interesting that a higher L5I in multi_lysis cases was found to be significantly higher than that observed in the mono_lysis cases, despite PI being similar between the 2 subgroups. It is possible that high L5I causes more tension at the pars interarticularis of supradjacent levels, where a shear stress mechanism7 likely results in additional spondylolysis. In brief, a higher PI was a risk factor for lumbosacral spondylolysis (L5). A higher L5I together with a high PI could cause even more tension on the pars interarticularis at L5, causing greater tension at the supradjacent level (L4) and even at the second supradjacent level (L3), thus resulting in multi_lysis.

To the best of our knowledge, elevated PI results in a greater LL, which increases shear stress in the pars interarticularis.7,9 As shown in this study, a high PI can generate high LL and L4–S1 SL in both the mono_lysis and multi_lysis groups. However, LDI for both the spondylolysis subgroups was significantly lower than what was observed in the healthy control group. Similar to what is described in the literature, approximately two-thirds of LL occurs from the L4 to S1 segments in healthy subjects.29 Findings from this study highlighted that the loss of LL in the spondylolysis group mainly occurs in the lumbosacral region, more so in the multi_lysis group than in the mono_lysis group (59% ± 21% vs 64% ± 12%, p = 0.012). The lack of lower LL is one of the primary causes of sagittal malalignment.22,30

Furthermore, our work showed that sagittal malalignment in spondylolysis patients was anterior due to insufficient LL in lower lumbar alignment. To compensate for the trunk tilting forward, compensatory mechanisms such as thoracic flattening, adjacent mobile segments in the upper lumbar spine, and pelvic retroversion are enhanced.6,22 However, there is a maximum limit of compensatory mechanisms that can be achieved. For example, a significantly lower TK in the spondylolysis group than in the control group, with no statistically significant differences between the spondylolysis subgroups, revealed a limit of the thoracic flattening mechanism. It should also be highlighted that an unbalanced pelvis was observed in more patients in the multi_lysis group than in the mono_lysis group (54.9% vs 40.8%, p = 0.039) due to limitations in pelvic retroversion compensation. These limited compensatory mechanisms are insufficient to correct for anterior malalignment, leading to more cases of multi_lysis with a sagittal imbalance of the spine compared with what is seen in mono_lysis cases (29.4% vs 13.7%, p = 0.003).

Sagittal alignment is known to influence functional and clinical reported outcomes.11 Multilevel spondylolytic spondylolisthesis may have certain cumulative effects on slip degrees, loss of LL, pelvic retroversion, and related sagittal malalignment. The global sagittal malalignment of multi_lysis can lead to an array of symptoms that compromise QOL.11 High stress at the lumbosacral region results in disc degeneration,10 additive effects of multisegmental instability, or lumbar spinal stenosis,2,10,31 which may ultimately lead to worse QOL outcomes in multi_lysis patients versus mono_lysis patients, including in this study.

This study has two major strengths. First, the loss of LL in the multi_lysis group, mainly occurring at the lumbosacral region, suggests that restoration of lordosis in the L4–S1 region is a priority for a lumbar surgical treatment algorithm.32 Biomechanically, the shear forces at the adjacent segment are significantly higher in patients with inadequate restoration of lordosis in the lower lumbar spine.15 Inadequate restoration of lordosis in the L4–S1 region is a strong risk factor for adjacent-segment disease.32 Second, patients with pelvic retroversion compensation, particularly for an unbalanced pelvis, should focus on the maintenance and the restoration of normal pelvic balance through lumbar reconstructive procedures. Hresko et al.23 suggested that surgical reduction might be considered for patients exhibiting an unbalanced pelvis. Alzakri and colleagues33 further demonstrated that achieving normal pelvic balance postoperatively in high-grade spondylolisthesis cases was associated with better improvement in QOL. As demonstrated in the novel global alignment and proportion score,12 spinopelvic malalignment of unharmonious LDI and relative pelvic version in the spondylolysis group should be aligned in lumbar fusion surgery to reduce mechanical complication rates and improve long-term QOL.13 Based on our data, surgical strategies, such as release of the surrounding soft tissue to increase the rate of slip reduction, inserting a cage to restore the height of the intervertebral space, and insertion of a full bone graft for solid fusion, should be considered to correct lumbosacral deformities and sagittal spinal malalignment.

While there are several strengths, this study also has several limitations. For one, this was a retrospective study conducted using a single-center database, and thus this work needs to be repeated in other centers with different patient groups. Second, the natural history of the multi_lysis could not be identified in patients. Next, spinopelvic sagittal alignment at different positions was not thoroughly evaluated. Lastly, other potential confounding factors for sagittal alignment, such as stenosis, were not analyzed. However, this study, which described the sagittal malalignment in spondylolytic spondylolisthesis cases, included a large proportion of patients with multi_lysis.

Conclusions

There was an 11.3% incidence rate of multi_lysis in patients with symptomatic spondylolytic spondylolisthesis observed in this study. A high-PI pattern of spinopelvic sagittal alignment was associated with the occurrence of spondylolysis (both mono_lysis and multi_lysis), and high L5I may be associated with the development of consecutive multi_lysis. In contrast to mono_lysis cases, more multi_lysis cases showed anterior global malalignment with insufficient lower LL and an unbalanced pelvis. These findings emphasize the need for an adapted surgical correction in spondylolysis patients with distinct sagittal spinal malalignment, particularly in those exhibiting the characteristics of multi_lysis.

Acknowledgments

This work was supported by the National Natural Science Foundation of China (grant no. 81772422) and the Natural Science Foundation of Jiangsu Province (BE2017606 and BK20170126).

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Sun, Zhou, Wang, Qiu. Acquisition of data: Sun, Zhou, Qian, Zhu, Wang, Qiu. Analysis and interpretation of data: Sun, Zhou, Xu, Qiu. Drafting the article: Sun, Zhou, Qiu. Critically revising the article: Sun, Zhou, Chen, Qian, Zhu, Wang. Reviewed submitted version of manuscript: Sun, Zhou, Xu, Qian, Zhu, Wang. Approved the final version of the manuscript on behalf of all authors: Sun. Statistical analysis: Sun, Zhou, Xu. Administrative/technical/material support: Sun, Zhou. Study supervision: Sun, Zhou, Chen, Qian.

References

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  • 2

    He LC, Wang YX, Gong JS, et al. Prevalence and risk factors of lumbar spondylolisthesis in elderly Chinese men and women. Eur Radiol. 2014;24(2):441448.

    • Search Google Scholar
    • Export Citation
  • 3

    Belfi LM, Ortiz AO, Katz DS. Computed tomography evaluation of spondylolysis and spondylolisthesis in asymptomatic patients. Spine (Phila Pa 1976). 2006;31(24):E907E910.

    • Search Google Scholar
    • Export Citation
  • 4

    Sakai T, Sairyo K, Takao S, et al. Incidence of lumbar spondylolysis in the general population in Japan based on multidetector computed tomography scans from two thousand subjects. Spine (Phila Pa 1976). 2009;34(21):23462350.

    • Search Google Scholar
    • Export Citation
  • 5

    Endler P, Ekman P, Möller H, Gerdhem P. Outcomes of posterolateral fusion with and without instrumentation and of interbody fusion for isthmic spondylolisthesis: a prospective study. J Bone Joint Surg Am. 2017;99(9):743752.

    • Search Google Scholar
    • Export Citation
  • 6

    Labelle H, Mac-Thiong JM, Roussouly P. Spino-pelvic sagittal balance of spondylolisthesis: a review and classification. Eur Spine J. 2011;20(suppl 5):641646.

    • Search Google Scholar
    • Export Citation
  • 7

    Roussouly P, Gollogly S, Berthonnaud E, et al. Sagittal alignment of the spine and pelvis in the presence of L5-S1 isthmic lysis and low-grade spondylolisthesis. Spine (Phila Pa 1976). 2006;31(21):24842490.

    • Search Google Scholar
    • Export Citation
  • 8

    Labelle H, Roussouly P, Berthonnaud E, et al. Spondylolisthesis, pelvic incidence, and spinopelvic balance: a correlation study. Spine (Phila Pa 1976). 2004;29(18):20492054.

    • Search Google Scholar
    • Export Citation
  • 9

    Sterba M, Arnoux PJ, Labelle H, et al. Biomechanical analysis of spino-pelvic postural configurations in spondylolysis subjected to various sport-related dynamic loading conditions. Eur Spine J. 2018;27(8):20442052.

    • Search Google Scholar
    • Export Citation
  • 10

    Toy JO, Tinley JC, Eubanks JD, et al. Correlation of sacropelvic geometry with disc degeneration in spondylolytic cadaver specimens. Spine (Phila Pa 1976). 2012;37(1):E10E15.

    • Search Google Scholar
    • Export Citation
  • 11

    Harroud A, Labelle H, Joncas J, Mac-Thiong JM. Global sagittal alignment and health-related quality of life in lumbosacral spondylolisthesis. Eur Spine J. 2013;22(4):849856.

    • Search Google Scholar
    • Export Citation
  • 12

    Yilgor C, Sogunmez N, Boissiere L, et al. Global alignment and proportion (GAP) score: development and validation of a new method of analyzing spinopelvic alignment to predict mechanical complications after adult spinal deformity surgery. J Bone Joint Surg Am. 2017;99(19):16611672.

    • Search Google Scholar
    • Export Citation
  • 13

    Yilgor C, Sogunmez N, Yavuz Y, et al. Relative lumbar lordosis and lordosis distribution index: individualized pelvic incidence-based proportional parameters that quantify lumbar lordosis more precisely than the concept of pelvic incidence minus lumbar lordosis. Neurosurg Focus. 2017;43(6):E5.

    • Search Google Scholar
    • Export Citation
  • 14

    Rothenfluh DA, Mueller DA, Rothenfluh E, Min K. Pelvic incidence-lumbar lordosis mismatch predisposes to adjacent segment disease after lumbar spinal fusion. Eur Spine J. 2015;24(6):12511258.

    • Search Google Scholar
    • Export Citation
  • 15

    Senteler M, Weisse B, Snedeker JG, Rothenfluh DA. Pelvic incidence-lumbar lordosis mismatch results in increased segmental joint loads in the unfused and fused lumbar spine. Eur Spine J. 2014;23(7):13841393.

    • Search Google Scholar
    • Export Citation
  • 16

    Liu X, Wang L, Yuan S, et al. Multiple-level lumbar spondylolysis and spondylolisthesis. J Neurosurg Spine. 2015;22(3):283287.

  • 17

    Wu XD, Wang XW, Chen HJ, et al. Twenty-nine-year follow-up of nonoperatively treated three-level lumbar spondylolysis: a case report and review of the literature. JBJS Case Connect. 2016;6(1):e13.

    • Search Google Scholar
    • Export Citation
  • 18

    Wáng YXJ, Deng M, Griffith JF, et al. Lumbar spondylolisthesis progression and de novo spondylolisthesis in elderly Chinese men and women: a year-4 follow-up study. Spine (Phila Pa 1976). 2016;41(13):10961103.

    • Search Google Scholar
    • Export Citation
  • 19

    Oh SK, Chung SS, Lee CS. Correlation of pelvic parameters with isthmic spondylolisthesis. Asian Spine J. 2009;3(1):2126.

  • 20

    Duval-Beaupère G, Schmidt C, Cosson P. A barycentremetric study of the sagittal shape of spine and pelvis: the conditions required for an economic standing position. Ann Biomed Eng. 1992;20(4):451462.

    • Search Google Scholar
    • Export Citation
  • 21

    Ferrero E, Ould-Slimane M, Gille O, Guigui P. Sagittal spinopelvic alignment in 654 degenerative spondylolisthesis. Eur Spine J. 2015;24(6):12191227.

    • Search Google Scholar
    • Export Citation
  • 22

    Ferrero E, Simon AL, Magrino B, et al. Double-level degenerative spondylolisthesis: what is different in the sagittal plane? Eur Spine J. 2016;25(8):25462552.

    • Search Google Scholar
    • Export Citation
  • 23

    Hresko MT, Labelle H, Roussouly P, Berthonnaud E. Classification of high-grade spondylolistheses based on pelvic version and spine balance: possible rationale for reduction. Spine (Phila Pa 1976). 2007;32(20):22082213.

    • Search Google Scholar
    • Export Citation
  • 24

    Zhu F, Bao H, Liu Z, et al. Analysis of L5 incidence in normal population use of L5 incidence as a guide in reconstruction of lumbosacral alignment. Spine (Phila Pa 1976). 2014;39(2):E140E146.

    • Search Google Scholar
    • Export Citation
  • 25

    Schwab F, Ungar B, Blondel B, et al. Scoliosis Research Society-Schwab adult spinal deformity classification: a validation study. Spine (Phila Pa 1976). 2012;37(12):10771082.

    • Search Google Scholar
    • Export Citation
  • 26

    Ravichandran G. Multiple lumbar spondylolyses. Spine (Phila Pa 1976). 1980;5(6):552557.

  • 27

    Park SJ, Lee CS, Chung SS, et al. Postoperative changes in pelvic parameters and sagittal balance in adult isthmic spondylolisthesis. Neurosurgery. 2011;68(2)(Suppl Operative):355–363.

    • Search Google Scholar
    • Export Citation
  • 28

    Mehta VA, Amin A, Omeis I, et al. Implications of spinopelvic alignment for the spine surgeon. Neurosurgery. 2012;70(3):707721.

  • 29

    Hey HWD, Lau ET, Tan KA, et al. Lumbar spine alignment in six common postures: an ROM analysis with implications for deformity correction. Spine (Phila Pa 1976). 2017;42(19):14471455.

    • Search Google Scholar
    • Export Citation
  • 30

    Uehara M, Takahashi J, Ikegami S, et al. Sagittal spinal alignment deviation in the general elderly population: a Japanese cohort survey randomly sampled from a basic resident registry. Spine J. 2019;19(2):349356.

    • Search Google Scholar
    • Export Citation
  • 31

    McCunniff PT, Yoo H, Dugarte A, et al. Bilateral pars defects at the L4 vertebra result in increased degeneration when compared with those at L5: an anatomic study. Clin Orthop Relat Res. 2016;474(2):571577.

    • Search Google Scholar
    • Export Citation
  • 32

    Berven S, Wadhwa R. Sagittal alignment of the lumbar spine. Neurosurg Clin N Am. 2018;29(3):331339.

  • 33

    Alzakri A, Labelle H, Hresko MT, et al. Restoration of normal pelvic balance from surgical reduction in high-grade spondylolisthesis. Eur Spine J. 2019;28:20872094.

    • Search Google Scholar
    • Export Citation

Illustration from Matsukawa et al. (186–191). Left panel: Copyright Medical View Co., Ltd. Published with permission.

  • View in gallery

    Representative lateral radiographs obtained in a patient with double-level spondylolysis (A), a patient with mono_lysis (B), and a healthy individual (C). A: A 59-year-old female with L4–5 and L5–S1 double-level spondylolysis. PI = 70.6°, PT/PI ratio = 42%, L5I = 57.0°, LL = 45.20°, LDI = 16%, SVA = 92 mm. B: A 52-year-old female with L5–S1 mono_lysis. PI = 56.1°, PT/PI ratio = 30.4%, L5I = 25.7°, LL = 57.4°, LDI = 63%, SVA = 9 mm. C: A 46-year-old healthy individual without back pain. PI = 44.3°, PT/PI ratio = 16%, L5I = 14.1°, LL = 52°, LDI = 74%, SVA = −12 mm.

  • View in gallery

    Radiological parameters measured on upright radiographs. A: Pelvic parameters: PI, PT, SS, and L5I. B: Slip parameters: slip angle (α), slip percentage (line bc/line ac × 100%). C: Sagittal alignment parameters: L4–S1 segmental lordosis (L4–S1 SL), LL, TK, and SVA.

  • View in gallery

    Comparison of sagittal alignment parameters between the control group and the spondylolysis group.

  • 1

    Fredrickson BE, Baker D, McHolick WJ, et al. The natural history of spondylolysis and spondylolisthesis. J Bone Joint Surg Am. 1984;66(5):699707.

    • Search Google Scholar
    • Export Citation
  • 2

    He LC, Wang YX, Gong JS, et al. Prevalence and risk factors of lumbar spondylolisthesis in elderly Chinese men and women. Eur Radiol. 2014;24(2):441448.

    • Search Google Scholar
    • Export Citation
  • 3

    Belfi LM, Ortiz AO, Katz DS. Computed tomography evaluation of spondylolysis and spondylolisthesis in asymptomatic patients. Spine (Phila Pa 1976). 2006;31(24):E907E910.

    • Search Google Scholar
    • Export Citation
  • 4

    Sakai T, Sairyo K, Takao S, et al. Incidence of lumbar spondylolysis in the general population in Japan based on multidetector computed tomography scans from two thousand subjects. Spine (Phila Pa 1976). 2009;34(21):23462350.

    • Search Google Scholar
    • Export Citation
  • 5

    Endler P, Ekman P, Möller H, Gerdhem P. Outcomes of posterolateral fusion with and without instrumentation and of interbody fusion for isthmic spondylolisthesis: a prospective study. J Bone Joint Surg Am. 2017;99(9):743752.

    • Search Google Scholar
    • Export Citation
  • 6

    Labelle H, Mac-Thiong JM, Roussouly P. Spino-pelvic sagittal balance of spondylolisthesis: a review and classification. Eur Spine J. 2011;20(suppl 5):641646.

    • Search Google Scholar
    • Export Citation
  • 7

    Roussouly P, Gollogly S, Berthonnaud E, et al. Sagittal alignment of the spine and pelvis in the presence of L5-S1 isthmic lysis and low-grade spondylolisthesis. Spine (Phila Pa 1976). 2006;31(21):24842490.

    • Search Google Scholar
    • Export Citation
  • 8

    Labelle H, Roussouly P, Berthonnaud E, et al. Spondylolisthesis, pelvic incidence, and spinopelvic balance: a correlation study. Spine (Phila Pa 1976). 2004;29(18):20492054.

    • Search Google Scholar
    • Export Citation
  • 9

    Sterba M, Arnoux PJ, Labelle H, et al. Biomechanical analysis of spino-pelvic postural configurations in spondylolysis subjected to various sport-related dynamic loading conditions. Eur Spine J. 2018;27(8):20442052.

    • Search Google Scholar
    • Export Citation
  • 10

    Toy JO, Tinley JC, Eubanks JD, et al. Correlation of sacropelvic geometry with disc degeneration in spondylolytic cadaver specimens. Spine (Phila Pa 1976). 2012;37(1):E10E15.

    • Search Google Scholar
    • Export Citation
  • 11

    Harroud A, Labelle H, Joncas J, Mac-Thiong JM. Global sagittal alignment and health-related quality of life in lumbosacral spondylolisthesis. Eur Spine J. 2013;22(4):849856.

    • Search Google Scholar
    • Export Citation
  • 12

    Yilgor C, Sogunmez N, Boissiere L, et al. Global alignment and proportion (GAP) score: development and validation of a new method of analyzing spinopelvic alignment to predict mechanical complications after adult spinal deformity surgery. J Bone Joint Surg Am. 2017;99(19):16611672.

    • Search Google Scholar
    • Export Citation
  • 13

    Yilgor C, Sogunmez N, Yavuz Y, et al. Relative lumbar lordosis and lordosis distribution index: individualized pelvic incidence-based proportional parameters that quantify lumbar lordosis more precisely than the concept of pelvic incidence minus lumbar lordosis. Neurosurg Focus. 2017;43(6):E5.

    • Search Google Scholar
    • Export Citation
  • 14

    Rothenfluh DA, Mueller DA, Rothenfluh E, Min K. Pelvic incidence-lumbar lordosis mismatch predisposes to adjacent segment disease after lumbar spinal fusion. Eur Spine J. 2015;24(6):12511258.

    • Search Google Scholar
    • Export Citation
  • 15

    Senteler M, Weisse B, Snedeker JG, Rothenfluh DA. Pelvic incidence-lumbar lordosis mismatch results in increased segmental joint loads in the unfused and fused lumbar spine. Eur Spine J. 2014;23(7):13841393.

    • Search Google Scholar
    • Export Citation
  • 16

    Liu X, Wang L, Yuan S, et al. Multiple-level lumbar spondylolysis and spondylolisthesis. J Neurosurg Spine. 2015;22(3):283287.

  • 17

    Wu XD, Wang XW, Chen HJ, et al. Twenty-nine-year follow-up of nonoperatively treated three-level lumbar spondylolysis: a case report and review of the literature. JBJS Case Connect. 2016;6(1):e13.

    • Search Google Scholar
    • Export Citation
  • 18

    Wáng YXJ, Deng M, Griffith JF, et al. Lumbar spondylolisthesis progression and de novo spondylolisthesis in elderly Chinese men and women: a year-4 follow-up study. Spine (Phila Pa 1976). 2016;41(13):10961103.

    • Search Google Scholar
    • Export Citation
  • 19

    Oh SK, Chung SS, Lee CS. Correlation of pelvic parameters with isthmic spondylolisthesis. Asian Spine J. 2009;3(1):2126.

  • 20

    Duval-Beaupère G, Schmidt C, Cosson P. A barycentremetric study of the sagittal shape of spine and pelvis: the conditions required for an economic standing position. Ann Biomed Eng. 1992;20(4):451462.

    • Search Google Scholar
    • Export Citation
  • 21

    Ferrero E, Ould-Slimane M, Gille O, Guigui P. Sagittal spinopelvic alignment in 654 degenerative spondylolisthesis. Eur Spine J. 2015;24(6):12191227.

    • Search Google Scholar
    • Export Citation
  • 22

    Ferrero E, Simon AL, Magrino B, et al. Double-level degenerative spondylolisthesis: what is different in the sagittal plane? Eur Spine J. 2016;25(8):25462552.

    • Search Google Scholar
    • Export Citation
  • 23

    Hresko MT, Labelle H, Roussouly P, Berthonnaud E. Classification of high-grade spondylolistheses based on pelvic version and spine balance: possible rationale for reduction. Spine (Phila Pa 1976). 2007;32(20):22082213.

    • Search Google Scholar
    • Export Citation
  • 24

    Zhu F, Bao H, Liu Z, et al. Analysis of L5 incidence in normal population use of L5 incidence as a guide in reconstruction of lumbosacral alignment. Spine (Phila Pa 1976). 2014;39(2):E140E146.

    • Search Google Scholar
    • Export Citation
  • 25

    Schwab F, Ungar B, Blondel B, et al. Scoliosis Research Society-Schwab adult spinal deformity classification: a validation study. Spine (Phila Pa 1976). 2012;37(12):10771082.

    • Search Google Scholar
    • Export Citation
  • 26

    Ravichandran G. Multiple lumbar spondylolyses. Spine (Phila Pa 1976). 1980;5(6):552557.

  • 27

    Park SJ, Lee CS, Chung SS, et al. Postoperative changes in pelvic parameters and sagittal balance in adult isthmic spondylolisthesis. Neurosurgery. 2011;68(2)(Suppl Operative):355–363.

    • Search Google Scholar
    • Export Citation
  • 28

    Mehta VA, Amin A, Omeis I, et al. Implications of spinopelvic alignment for the spine surgeon. Neurosurgery. 2012;70(3):707721.

  • 29

    Hey HWD, Lau ET, Tan KA, et al. Lumbar spine alignment in six common postures: an ROM analysis with implications for deformity correction. Spine (Phila Pa 1976). 2017;42(19):14471455.

    • Search Google Scholar
    • Export Citation
  • 30

    Uehara M, Takahashi J, Ikegami S, et al. Sagittal spinal alignment deviation in the general elderly population: a Japanese cohort survey randomly sampled from a basic resident registry. Spine J. 2019;19(2):349356.

    • Search Google Scholar
    • Export Citation
  • 31

    McCunniff PT, Yoo H, Dugarte A, et al. Bilateral pars defects at the L4 vertebra result in increased degeneration when compared with those at L5: an anatomic study. Clin Orthop Relat Res. 2016;474(2):571577.

    • Search Google Scholar
    • Export Citation
  • 32

    Berven S, Wadhwa R. Sagittal alignment of the lumbar spine. Neurosurg Clin N Am. 2018;29(3):331339.

  • 33

    Alzakri A, Labelle H, Hresko MT, et al. Restoration of normal pelvic balance from surgical reduction in high-grade spondylolisthesis. Eur Spine J. 2019;28:20872094.

    • Search Google Scholar
    • Export Citation

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