Subtle segmental angle changes of single-level lumbar fusions and adjacent-level biomechanics: cadaveric study of optically measured disc strain

Bernardo de Andrada Pereira Spinal Biomechanics Laboratory, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix; and

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Piyanat Wangsawatwong Spinal Biomechanics Laboratory, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix; and

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Jennifer N. Lehrman Spinal Biomechanics Laboratory, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix; and

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Anna G. U. Sawa Spinal Biomechanics Laboratory, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix; and

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S. Harrison Farber Department of Neurosurgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, Arizona

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Jakub Godzik Department of Neurosurgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, Arizona

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Luke K. O’Neill Spinal Biomechanics Laboratory, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix; and

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Juan S. Uribe Department of Neurosurgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, Arizona

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Brian P. Kelly Spinal Biomechanics Laboratory, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix; and

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Jay D. Turner Department of Neurosurgery, Barrow Neurological Institute, St. Joseph’s Hospital and Medical Center, Phoenix, Arizona

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OBJECTIVE

Changes to segmental lordosis at a single level may affect adjacent-level biomechanics and overall spinal alignment with an iatrogenic domino effect commonly seen in adult spinal deformity. This study investigated the effects of different segmental angles of single-level lumbar fixation on stability and principal strain across the surface of the adjacent-level disc.

METHODS

Seven human cadaveric L3–S1 specimens were instrumented at L4–5 and tested in 3 conditions: 1) neutral native angle ("neutral"), 2) increasing angle by 5° of lordosis ("lordosis"), and 3) decreasing angle by 5° of kyphosis ("kyphosis"). Pure moment loads (7.5 Nm) were applied in flexion, extension, lateral bending, and axial rotation, followed by 400 N of axial compression alone and together with pure moments. Range of motion (ROM), principal maximum strain (E1), and principal minimum strain (E2) across different surface subregions of the upper adjacent-level disc (L3–4) were optically assessed. Larger magnitudes of either E1 or E2 indicate larger tissue deformations and represent indirect measures of increased stress.

RESULTS

At the superior adjacent level, a significant increase in ROM was observed in kyphosis and lordosis versus neutral in flexion (p ≤ 0.001) and extension (p ≤ 0.02). ROM was increased in lordosis versus neutral (p = 0.03) and kyphosis (p = 0.004) during compression. ROM increased in kyphosis versus neutral and lordosis (both p = 0.03) in compression plus extension. Lordosis resulted in increased E1 across the midposterior subregion of the disc (Q3) versus neutral during right lateral bending (p = 0.04); lordosis and kyphosis resulted in decreased E1 in Q3 versus neutral with compression (p ≤ 0.03). Lordosis decreased E1 in Q3 versus neutral during compression plus flexion (p = 0.01), whereas kyphosis increased E1 in all quartiles and increased E2 in the midanterior subregion versus lordosis in compression plus flexion (p ≤ 0.047). Kyphosis decreased E1 in Q3 (p = 0.02) and E2 in the anterior-most subregion of the disc (Q1) (p = 0.006) versus neutral, whereas lordosis decreased E1 in Q3 (p = 0.008) versus neutral in compression plus extension.

CONCLUSIONS

Lumbar spine monosegmental fixation with 5° offset from the neutral individual segmental angle altered the motion and principal strain magnitudes at the upper adjacent disc, with induced kyphosis resulting in larger principal strains compared with lordosis. Segmental alignment of single-level fusion influences adjacent-segment biomechanics, and suboptimal alignment may play a role in the clinical development of adjacent-segment disease.

ABBREVIATIONS

ASD = adjacent-segment degeneration; DIC = digital image correlation; E1 = principal maximum strain; E2 = principal minimum strain; Q1 = anterior-most subregion of the disc; Q2 = midanterior subregion of the disc; Q3 = midposterior subregion of the disc; Q4 = posterior-most subregion of the disc; ROM = range of motion.

OBJECTIVE

Changes to segmental lordosis at a single level may affect adjacent-level biomechanics and overall spinal alignment with an iatrogenic domino effect commonly seen in adult spinal deformity. This study investigated the effects of different segmental angles of single-level lumbar fixation on stability and principal strain across the surface of the adjacent-level disc.

METHODS

Seven human cadaveric L3–S1 specimens were instrumented at L4–5 and tested in 3 conditions: 1) neutral native angle ("neutral"), 2) increasing angle by 5° of lordosis ("lordosis"), and 3) decreasing angle by 5° of kyphosis ("kyphosis"). Pure moment loads (7.5 Nm) were applied in flexion, extension, lateral bending, and axial rotation, followed by 400 N of axial compression alone and together with pure moments. Range of motion (ROM), principal maximum strain (E1), and principal minimum strain (E2) across different surface subregions of the upper adjacent-level disc (L3–4) were optically assessed. Larger magnitudes of either E1 or E2 indicate larger tissue deformations and represent indirect measures of increased stress.

RESULTS

At the superior adjacent level, a significant increase in ROM was observed in kyphosis and lordosis versus neutral in flexion (p ≤ 0.001) and extension (p ≤ 0.02). ROM was increased in lordosis versus neutral (p = 0.03) and kyphosis (p = 0.004) during compression. ROM increased in kyphosis versus neutral and lordosis (both p = 0.03) in compression plus extension. Lordosis resulted in increased E1 across the midposterior subregion of the disc (Q3) versus neutral during right lateral bending (p = 0.04); lordosis and kyphosis resulted in decreased E1 in Q3 versus neutral with compression (p ≤ 0.03). Lordosis decreased E1 in Q3 versus neutral during compression plus flexion (p = 0.01), whereas kyphosis increased E1 in all quartiles and increased E2 in the midanterior subregion versus lordosis in compression plus flexion (p ≤ 0.047). Kyphosis decreased E1 in Q3 (p = 0.02) and E2 in the anterior-most subregion of the disc (Q1) (p = 0.006) versus neutral, whereas lordosis decreased E1 in Q3 (p = 0.008) versus neutral in compression plus extension.

CONCLUSIONS

Lumbar spine monosegmental fixation with 5° offset from the neutral individual segmental angle altered the motion and principal strain magnitudes at the upper adjacent disc, with induced kyphosis resulting in larger principal strains compared with lordosis. Segmental alignment of single-level fusion influences adjacent-segment biomechanics, and suboptimal alignment may play a role in the clinical development of adjacent-segment disease.

In Brief

Investigators used a cadaveric model and a novel optical technology for digital imaging strain correlation to evaluate in vitro biomechanical effects on the adjacent level after a single-level fusion fixation at +5° (lordotic) or -5° (kyphotic) segmental angles compared with the native (neutral) angle. The results showed that fixation in kyphosis or lordosis can significantly affect the adjacent level. These results improve our understanding of adjacent-level disease pathogenesis and prevention in adult spinal deformity.

Incorporating spinopelvic parameters in the surgical restoration of sagittal balance improves clinical outcomes in spinal fusions, where the severity of symptoms increases in a linear fashion with progressive, positive sagittal plane deformity.1 For many years, single-level lumbar fusion was performed with little or no regard for the segmental angle at the index level of fixation or the consequences of fixation on the adjacent levels, regional lordosis, or ultimately overall global spinal alignment. Subtle changes to the segmental lordosis at a single level may affect adjacent-level biomechanics and ultimately the overall spinal alignment with an iatrogenic domino effect commonly seen in adult spinal deformity.

Relative kyphosis is poorly tolerated in the lumbar spine.1 The upper arc of the lumbar lordosis is more constant, whereas the lower arc is more variable and plays a greater role in overall lordosis, accounting for two-thirds of the total lumbar lordosis angle.26 The lower arc also corresponds with, and reacts to, the sacral slope angle and dictates the overall lumbar lordosis shape. Therefore, even minor changes in this region have the potential to dramatically affect the distribution of mechanical loading at adjacent levels. As such, single-level fusions performed across the lower lumbar spine should consider the final segmental angle to offset the development of adjacent-segment degeneration (ASD).

Previous work reported that the suboptimal restoration of focal lumbar lordosis in unstable low-grade spondylolisthesis is associated with ASD.7 Likewise, several studies have shown that fusion of the lumbar spine in abnormal sagittal alignment with loss of lumbar lordosis predisposes patients to the development of ASD.810 Zheng et al.11 reported that patients with a low postoperative lumbar distribution index, which measures the role of the lower lumbar lordotic arc (L4–S1) relative to the total lordosis, have a higher risk of developing ASD.

Authors have recently begun to explore the consequences of changing the segmental angle on global spinal alignment following single-level fusion and the biomechanical implications of undercorrection or overcorrection of lumbar lordosis on adjacent levels.1217 Little is currently known regarding how differences in focal lumbar lordosis, created by single-level posterior lumbar pedicle screw and rod fixation, affect adjacent-segment biomechanics, particularly with respect to intervertebral disc stress and strain distributions. Increased and/or redistributed intervertebral disc stress and strain may be averse to disc health and a precursor to clinical signs of ASD. This study investigated the biomechanical effects of different segmental angles of single-level pedicle screw and rod fixation in terms of stability and intervertebral disc strain at the upper (noninstrumented) adjacent level.

Methods

Specimen Preparations

Seven human cadaveric L3–S1 specimens were studied (Table 1). Donor medical records were reviewed to exclude bone disease and specimens with any obvious visible or radiographic osseous abnormality. Dual-energy x-ray absorptiometry scans were performed on the L4 vertebra of each specimen to assess bone mineral density. The mean (SD) bone mineral density was 0.929 (0.12) g/cm2. Specimens with osteoporosis (T-score less than −2.5 according to the World Health Organization) were excluded.

TABLE 1.

Specimen details

Specimen No.BMD, g/cm2SexAge, yrsCause of Death
10.907F20Unknown
20.988M49Unknown
30.990F35Cardiogenic shock
41.136F44Diabetes complication
50.842M32Pulmonary embolism
60.768M55Cerebrovascular disease
70.869M64Cardiovascular disease

BMD = bone mineral density.

Specimens were stored at −30°C until the day of testing. In preparation for testing, specimens were thawed in a bath of normal saline at room temperature (approximately 21°C) and carefully cleaned of muscle tissue without damaging any ligaments, discs, or joint capsules. Household screws were inserted in the sacrum, and these screw heads were embedded in a block of fast-curing resin (Smooth-Cast 300-Q, Smooth-On, Inc.) for rigid fixation to the base of the testing apparatus. Similarly, household screws were inserted in the L3 endplates, facet articulations, and spinous process, and these screw heads were potted in the same fast-curing resin to facilitate attachment to the testing apparatus for load application.

Surgical Instrumentation and Test Conditions

Polyaxial pedicle screws with a cobalt chrome head and titanium alloy shaft (Ti-6A1-4V) were then bilaterally inserted (NuVasive, Inc., 6.5 × 45–55 mm) from L4 to L5 under fluoroscopic guidance. Two 5.5-mm-diameter cobalt chrome rods were contoured bilaterally to smoothly fit screw heads without the need for screw-rod reduction. All specimens were tested in 3 instrumented conditions without an interbody device: 1) L4–5 pedicle screw and rod with neutral (natural) segmental angle ("neutral" condition); 2) L4–5 pedicle screw and rod with 5° of lordosis from the natural segmental angle, using the compressor tool on the bilateral pedicle screw tulip heads ("lordosis" condition); and 3) L4–5 pedicle screw and rod with 5° of kyphosis from the natural segmental angle, using the distractor tool on the bilateral pedicle screw tulip heads ("kyphosis" condition). Confirmation of the segmental Cobb angle change was obtained using lateral C-arm (OEC 9800, GE HealthCare) radiographic views, and the angle was measured using the iPhone iOS 14 Level Tool App (Apple, Inc.). The neutral, lordosis (+5°), and kyphosis (−5°) segmental angles are detailed in Table 2, and example radiographs from an instrumented specimen are displayed in Fig. 1.

TABLE 2.

Measured segmental angle in neutral, kyphosis (−5°), and lordosis (+5°) position in degrees

Specimen No.Neutral, °Kyphosis, °Lordosis, °
113818
2211626
3262131
4292434
514920
6221726
7272232
FIG. 1.
FIG. 1.

Lateral radiographs showing the L4–5 pedicle screw and rod instrumentation and conditions tested. A: Lordosis condition: 5° of lordosis added to the natural segmental angle, using the compressor tool on the bilateral pedicle screw tulip heads, resulting in 18° segmental lordosis. B: Neutral condition: natural segmental angle of 13°. C: Kyphosis condition: 5° of kyphosis added to the natural segmental angle, using the distractor tool on the bilateral pedicle screw tulip heads, resulting in 8° segmental kyphosis. Figure is available in color online only.

Biomechanical Pure Moment and Compression Testing

All specimens were subjected to pure moment flexibility tests applying nondestructive, nonconstraining torques via a 6-degrees-of-freedom robotic testing frame.18,19 While under load control, maximum pure moment loads of 7.5 Nm were applied to induce flexion, extension, left and right lateral bending, and left and right axial rotation by continuous dynamic loading of 3 cycles, at a loading rate of 1.5°/sec. Following pure moment testing, each specimen was loaded in axial compression at the specimen center of rotation such that no sagittal plane rotation was induced. Axial compression (400 N) was applied alone and in combination with 3 cycles of pure moments. Three-dimensional motion in response to the applied loads was captured using the Optotrak 3020 system (Northern Digital, Inc.), which measured the 3D displacement of infrared emitting markers that were rigidly attached to each vertebra in a noncollinear arrangement. Custom software then converted marker coordinates into individual local coordinate systems for each vertebra so that intervertebral (including adjacent-level L3–4) angular motion could be calculated.20,21 In all tests, rotational range of motion (ROM) was identified at the peak load during the third cycle of loading and recorded for statistical analysis.

Optical Strain via Direct Image Correlation Analysis

Before mounting each specimen in the test frame, the left lateral tissue surface—vertebral bodies and discs—was covered with dark blue food dye and then sprayed with white paint (Rust-Oleum 2X Painter’s Touch, Flat White; Rust-Oleum) to create a high-contrast speckled pattern (Fig. 2). A commercial 3D digital image correlation (DIC) system (VIC-3D, Correlated Solutions, Inc.)—including two 12.3 MP (4096 × 3000 pixels, 20 fps) digital cameras with Xenoplan 2.8/50 mm compact lenses (Schneider Kreuznach) and two LED lights (525 lm, 4100 K)—was used to track the movement of the 3D-speckled pattern on each specimen during each condition and direction of loading. Postprocessing capabilities within the DIC software were then used to convert the speckled-pattern movement into topographical maps of principal maximum strain (E1) and principal minimum strain (E2) across the analyzed surface at peak loads. The left lateral side of the L3–4 disc was further divided into 4 subregions of interest (anterior-most subregion of the disc [Q1]; midanterior subregion of the disc [Q2]; midposterior subregion of the disc [Q3]; posterior-most subregion of the disc [Q4] anteroposterior quarters; Fig. 3). VIC-3D software capabilities were used to extract mean principal strains (E1 and E2) for each subregion (Q1–Q4), specimen (n = 7), condition (neutral, lordosis, and kyphosis), and direction of loading (pure moments [flexion, extension, left and right lateral bending, and left and right axial rotation]; compression alone; and compression plus each pure moment load type). Figure 4 illustrates the DIC analysis of the adjacent-segment disc with different index-level angles in lordosis and kyphosis.

FIG. 2.
FIG. 2.

DIC layout and examples. A: Superior view of the layout for the DIC camera (left lateral) and Optotrak camera (right lateral) relative to the vertebral specimen. B: Photograph of a specimen mounted to a robotic test frame depicting the speckle pattern applied to soft tissue and bone on the anterior spinal column. C: Computer screenshot of analyzed speckle pattern using DIC software showing maximum principal strain distribution during the pure moment flexion test. Figure is available in color online only.

FIG. 3.
FIG. 3.

Intervertebral disc subregions of interest (anteroposterior quarters). Figure is available in color online only.

FIG. 4.
FIG. 4.

A and B: Illustrations representing models with different index-level angles (white lines) with 5° of lordosis (A) and 5° of kyphosis (B) from the native angle. The yellow boxes represent the adjacent-segment discs, where the DIC analyses were performed. C and D: DIC camera analysis of the adjacent-segment disc with different index-level angles in lordosis (C) and kyphosis (D) for a single-level L4–5 pedicle screw and rod fusion. Panels 4A and 4B used with permission from Barrow Neurological Institute, Phoenix, Arizona. Figure is available in color online only.

Interpreting Principal Surface Strains (E1 and E2) by Quadrants

Large magnitudes of E1, based on the optical separation of dots speckled on the disc surface, indicate local regions of tissue stretch induced by disc bulging (e.g., horizontally oriented direction of E1) or linear separation or lengthening (e.g., vertical E1). Conversely, large magnitudes of E2, based on dots speckled on the disc surface moving closer together, indicate local regions of tissue shrinking or narrowing (along a direction perpendicular to E2). For example, as a rubber band is stretched, it elongates in length while simultaneously narrowing along its width. Larger magnitudes of either E1 or E2 indicate larger tissue deformations during loading and represent indirect measures of increased tissue stress.

The intervertebral disc was separated into quadrants for analysis because values of E1 and E2 vary significantly between disc regions and are highly dependent on the direction of the applied load. For example, during flexion, the greatest changes in local disc height are toward the anterior and posterior borders, with height shortening and elongating, respectively. In addition, a healthy disc also tends to bulge (effectively stretching the surface) more toward the direction of bending. During flexion, it was anticipated that the Q1 region would experience both E1 (bulging) and E2 (shortening) strains, the Q4 region would experience primarily E1 strain (greatest elongation with little or no bulging), and Q2 and Q3 would experience intermediate E1 and E2.

Statistical Comparisons

Mean values and standard deviations of peak ROM and principal strains in each quarter Q1–Q4 among the 3 instrumented conditions per direction of loading were computed and statistically compared using one-way repeated-measures analysis of variance tests, followed by Holm-Šidák post hoc multiple comparisons (as needed). The statistical significance was set at p ≤ 0.05.

Results

Adjacent-Level (L3–4) ROM

All conditions (neutral, lordosis, and kyphosis) resulted in similar relative responses to the different directions of loading (Fig. 5) at the superior adjacent level (L3–4). A statistically significant increase in mean ROM was observed in both kyphosis and lordosis conditions compared with the neutral condition during flexion (kyphosis: +6% [0.31°], p = 0.001; lordosis: +7% [0.35°], p ≤ 0.001) and extension (kyphosis: +9% [0.2°], p = 0.02; lordosis: +11% [0.25°], p = 0.009). ROM was also greater with lordosis compared with neutral (+26% [0.46°], p = 0.03) and kyphosis (+42% [0.66°], p = 0.004) during compression. When compression plus pure moment loads were applied, kyphosis resulted in increased ROM compared with neutral (+13% [0.17°], p = 0.03) and lordosis +24% [0.32°], p = 0.03) during compression plus extension. Although these angular changes are small, they exceed the measurement resolution of our tracking system (maximum error, 0.1°).

FIG. 5.
FIG. 5.

Mean (SD) ROM for all load directions at L3–4, the superior adjacent level to instrumentation. #Statistically significant difference compared with kyphosis condition (p < 0.05). *Statistically significant difference compared with neutral condition (p < 0.05). C = compression; EX = extension; FL = flexion; LAR = left axial rotation; LLB = left lateral bending; RAR = right axial rotation; RLB = right lateral bending.

Adjacent-Level (L3–4) Principal Surface Strain

All conditions (neutral, lordosis, and kyphosis) resulted in similar changes in mean E1 and E2 at L3–4 in response to the direction of loading (Fig. 6). The descriptions of strain results are presented by pure moment loads, compression, and compression plus pure moment loads to facilitate comprehension.

FIG. 6.
FIG. 6.

Mean (SD) E1 and E2 per subregion of L3–4 disc (Q1, Q2, Q3, and Q4). #Statistically significant difference compared with lordosis condition (p < 0.05). *Statistically significant difference compared with neutral condition (p < 0.05).

Pure Moment Loads

One significant difference among conditions was seen during right lateral bending in Q3 when E1 was 46% greater with lordosis than with neutral (109,425 µε vs 74,707 µε, p = 0.04); E1 was also greater with kyphosis (39%) than with neutral but without statistical significance (p = 0.09). No other statistically significant difference was observed in pure moment loads for E1 or E2 for all quarters (p ≥ 0.04).

Compression

The lordosis and kyphosis conditions both resulted in a small (1042 µε and 28 µε, 12% and 0.1%, respectively) but statistically significant decrease in E1 compared with neutral in Q3 (p ≤ 0.03) in compression. No other statistically significant difference was observed in compression for E1 or E2 for all quarters (p ≥ 0.08).

Compression Plus Pure Moment Loads

When compression was applied with pure moment loads, most differences were seen during compression plus flexion, with E1 significantly greater in the kyphosis condition versus the lordosis condition in all subregions (Q1: 46,703 µε vs 30,035 µε [55%]; Q2: 21,183 µε vs 14,933 µε [42%]; Q3: 19,469 µε vs 13,818 µε [41%]; and Q4: 25,319 µε vs 16,757 µε [51%]; p ≤ 0.047). These significant E1 increases with kyphosis reflected an average increase of 50%. E1 in lordosis during compression plus flexion was less than that for the neutral condition in Q3 (13,818 µε vs 15,308 µε, p = 0.01). Both lordosis and kyphosis conditions resulted in a small (5% and 0.1%, respectively) but statistically significant decrease in magnitudes of E1 in Q3 during compression plus extension (lordosis 10,019 µε; kyphosis 10,496 µε vs neutral 10,530 µε, p ≤ 0.02). Lastly, E1 with lordosis was significantly smaller than with neutral and kyphosis (14% and 21%, respectively) in Q3 during compression plus right axial rotation (11,274 µε vs 13,102 µε [neutral] and 14,208 µε [kyphosis], p ≤ 0.048).

E2 magnitude with a kyphosis condition was also 32% greater than with a lordosis condition during compression plus flexion in Q1 to Q3, but only with statistical significance in Q2 (−47,317 µε vs −35,759 µε, p = 0.004). Also, during compression plus extension, E2 in Q1 was 48% smaller in magnitude with a kyphosis condition than with a neutral condition (−3597 µε vs −8381 µε, p = 0.006).

Discussion

Although the ideal alignment restoration remains partially unclear, it is well accepted that maintaining or restoring lumbar lordosis is a key for obtaining good outcomes in lumbar fusion surgery. Single-level lumbar fusion had been performed for years with little focus regarding the final segmental angle. Oftentimes, adjacent-level degeneration develops quickly following single-level lumbar fusion, and it is well accepted that nonideal final alignment is a risk factor for such degeneration. The lower arc of the lumbar lordosis curvature is particularly important structurally, because it correlates with the sacral slope angle and dictates the overall regional lordosis.26 Subtle changes in a native segmental angle in this angle-sensitive region may have the potential to dramatically affect the distribution of loads (stress distributions) on the adjacent levels and ultimately along the entire spine, pelvis, and lower limbs. Repeated occurrence of ASD in a patient who underwent revision surgery and cephalad extension of the fusion is usually associated with sagittal deformity and alignment issues. Loss of lumbar lordosis following spine fusion and decompensation of adjacent segments have the potential to activate postural compensatory mechanisms and are reportedly a cause of flat back syndrome and iatrogenic spinal deformity.22 These consequences could potentially be avoided if the segmental angle and spinal alignment are studied even for a single-level lumbar fusion with preserved remaining levels. The objective of our study was to quantify changes in the gold-standard adjacent-segment ROM as well as the new metric of intervertebral disc surface strain change with different segmental angles after single-level lumbar fusion, using an optical strain measurement tool. Understanding strain distribution may help to elucidate an underlying biomechanical cause of failure for many postoperative complications such as pseudarthrosis, instrumentation failure, ASD, and iatrogenic deformity with proximal junctional kyphosis. Investigating motion and the strain distribution on the adjacent disc superior to a fusion can help to elucidate the effects of altering the segmental angle with a single-level fusion on the adjacent-level mechanics.

The addition of 400 N of compression with the objective to simulate the upper-body weight brought changes in the strain not observed with only pure moment loading. Traditionally, biomechanical tests use pure moment alone to facilitate standardization and to simplify testing and analysis due to a uniformly distributed load across all spinal levels tested.18 This method, while useful for comparative ROM and stability testing, does not take into account other types of loads known to occur in vivo, such as constant gravitational loading due to upper-body weight, and thus, it may not reliably reproduce physiological stresses and strains that occur in vivo.

In our study, increased sagittal plane ROM was observed under pure moment loads at the superior adjacent level when the fused-level neutral alignment was increased or decreased by 5°. When 400 N of compression was applied together with pure moment loads to simulate the physiological condition of bending while accounting for upper-body weight, fixation in 5° kyphotic offset demonstrated increased motion compared with a neutral native angle and 5° of lordotic offset, with statistical significance in compression plus extension. No differences in ROM were observed in lateral bending or axial rotation. Although these adjacent-level ROM changes were statistically significant, they were generally small in magnitude (≤ 0.66°). Previous biomechanical studies have shown that an isolated spinal joint exhibits a greater ROM when tested with few or no adjacent segments than when tested as part of a longer intact spinal segment with multiple adjacent segments.23,24 In the current study, fixation at the index level in combination with posterior compression or distraction may have served to disrupt anterior or posterior annular and ligamentous tension and continuity across the specimen, such that the superior index level exhibited ROM more similar to that of an isolated spinal joint.

In spine biomechanics research, the strain has been traditionally measured using strain gauges on rigid bony or metal surfaces. However, this method is limited by the very small surface area of the application of the strain gauges. Strain gauges cannot be used to measure the deformations of soft tissue, as the gauges are not elastic enough to stretch with the soft tissue. The gauges would prevent the tissue from stretching normally at the attachment site and hence not register the tissue strains accurately.25 DIC strain analysis is a technique in which a series of high-resolution images of a speckled surface throughout a loading cycle are captured and computationally analyzed. Engineering strain measurements are calculated on the basis of the relative localized displacement of irregular speckle patterns on the surface of a test specimen. DIC analysis provides expanded surface analysis; however, because it is an optical technique, measurements are possible on visible surfaces only.26 Previous work demonstrated that the strain distribution on the surface of an entire spine segment could be measured with sufficient accuracy with the DIC method.27

We used DIC techniques to assess principal surface strains across the lateral human L3–4 disc, demonstrating for the first time that slight variations of a single-segment lumbar fusion angle can significantly alter the magnitude of mean principal intervertebral disc strains superior to a single-level lumbar pedicle screw and rod fixation. The noted significant variations in E1 and E2 across the different anteroposterior intervertebral disc subregions with different directions of loading (with and without compression) are indicators of significant variations in adjacent-level stress distributions, which have not been previously quantified experimentally in this manner.

Significant strain changes on the adjacent-level disc surface were observed during the pure moment test alone. With 5° of lordosis, the mean E1 increased by 46% during right lateral bending in the midposterior disc region compared with the native angle. During compression alone, very small but statistically significant decreases in E1 at the same region of the disc were observed for both 5° of kyphosis and lordosis—0.1% and 12%, respectively—compared with a native angle. When compression and flexion were applied together, a significant 50% increase in E1 occurred on the entire lateral surface of the adjacent-level disc when 5° of kyphosis was applied compared with 5° of lordosis. This was paired with increased E2 for the same load condition with significance in Q2. The remaining significant differences tended to be smaller in magnitude. Despite some significant decreases in strain on the adjacent-level discs in certain types of load tests, those changes had lower magnitudes and were more focal when compared with those increases in strain observed at this same disc. Overall, the strain analysis demonstrated an increase in adjacent-level disc strain with a postfixation segmental angle 5° offset for either kyphosis or lordosis. These changes were more substantial with kyphosis than lordosis and were load dependent.

The alignment changes applied in our study significantly altered strain and, therefore, stress distributions in the adjacent disc, which may pose a risk for disc health. The marked strain changes observed in kyphosis and the potential consequences to the adjacent-level disc are not easily extrapolated to the clinical level. However, previous clinical and laboratory studies have suggested that focal fixation in kyphosis or hypolordosis predisposes adjacent-level degeneration and, potentially, the domino effect of iatrogenic adult spinal deformity.8,11,2831 Driving the neutral, native segmental angle toward a different angle to maintain global or regional alignment in kyphosis or lordosis creates a tendency on the adjacent level to compensate for that angle change during motion. We suggest that this phenomenon is likely why both kyphosis and lordosis showed increased ROM in our study. There are two aspects to a lordotic correction—a global consideration and a segmental consideration. If the surgical goal is to achieve global alignment and sagittal balance, then this situation could have a positive benefit. However, this benefit could result in more local strain or an increase in ROM at the first superior level. Surgeons must be aware that monosegment or short-segment fixation should necessarily respect the natural spine curvature, although frequently, the segmental angle has been altered by degenerative disease by the time of the diagnosis. As proposed by Roussouly et al.,3 understanding a normal person’s healthy curvatures to restore the most physiological segmental native angle and the most physiological lumbar curvature should be pursued.

Zheng et al.11 investigated the relationship between postoperative lumbar lordosis distribution index (lower lumbar lordosis/overall lumbar lordosis × 100%) and symptomatic ASD in 200 patients and found that those with a low postoperative index (< 0.5), meaning less lordotic lower arc, were at greater risk of developing ASD. Findings in the patients in that study differed from those in the specimens in the current study model because the patients in Zheng and colleagues’ study were treated with an L4–S1 posterior lumbar interbody fusion rather than with a single-level fusion, but the concept that postfixation hypolordosis is not desired agrees with the findings of the present study. Similarly, in 1999, Oda et al.28 conducted an in vivo biomechanical experiment in a sheep model and reported that postoperative lumbar kyphotic deformity is associated with adjacent-level increased lamina strain and histological changes suggestive of degenerative osteoarthritis of the facet joints. Menezes-Reis et al.29 conducted a clinical analysis of 70 asymptomatic subjects and reported that the lumbar spines with hypolordotic shapes, more specifically Roussouly type II lumbar spines,3 are typically associated with early disc degeneration at the L4–5 level. These authors conjectured that, on flat lumbar spines, contact forces primarily act on the anterior column. In line with this conjecture, the current study found an increase in the anterior spinal column stress with a more kyphotic final angle.

Djurasovic et al.8 performed a case-control study of 51 patients with ASD and suggested that fusion of the lumbar spine with loss of lordosis would predispose patients to ASD. Zhao et al.30 conducted a finite element analysis of a lumbar spine L4–5 transforaminal lumbar interbody fusion model and reported that a decrease in lordosis generally increased the ROM and intradiscal pressure at the adjacent level, suggesting that decreased spinal lordosis poses stress at the adjacent segment and predisposes a patient to ASD.

Molz et al.32 performed a biomechanical study using two-level T12–L2 fixation in T10–S1 specimens under a 10-Nm load with neutral, kyphotic, and lordotic fusion alignments. At levels caudal to the fusion, they found increased ROM in kyphosis and lordosis but no difference between kyphosis and lordosis. The absence of any compressive load, as well as artifact loads from nonideal parallel cable and pulley alignments, could have influenced the results. They further did not characterize ROM at the adjacent cranial levels. Umehara et al.31 studied induced kyphosis across L4–S1 in L1–S1 cadaver segments during axial and extension loading. They found that induced kyphosis increased the load on the fusion instrumentation and increased local laminar strain at the upper adjacent vertebra. They did not report ROM changes or intervertebral disc strain changes.

Limitations

As with other biomechanical cadaveric studies, our testing paradigm evaluated only immediate stability and strain distributions. The principal strains evaluated were intervertebral disc-surface strains only. Cyclic loading was beyond the scope of this research and is problematic in vitro because of tissue degradation, which prevents simulation of the long-term in vivo loading environment before the occurrence of any instrumentation failure. Additional limitations include the absence of paraspinal and trunk muscle activity, which plays a role in stabilizing the lumbar spine, and the absence of a targeted disease, such as a segment with degenerative disease. We performed L4–5 pedicle screw and rod fusion without any interbody device, and the results could be altered with different types of commonly used interbody devices. We used the terms kyphosis and lordosis to didactically explain the direction of the segmental angle change in the sagittal plane. However, because we analyzed a lordotic region of the spine with subtle angle changes (5°), specimens could be considered to change from lordosis to less lordosis (−5°) or more lordosis (+5°) (Table 2). Other limitations include a lack of spinopelvic angle data, Roussouly classification type, and sagittal alignment parameters. These limitations represent challenges when performing cadaveric studies for logistic reasons, such as when the donor medical record lacks standing scoliosis radiographs.

Conclusions

Subtle segmental angle changes after single-level lumbar fusion from the native angle significantly affect adjacent-segment biomechanics, increasing motion and altering disc-surface strain distribution in a cadaveric model. The final offset angle in kyphosis induces more strain changes at the adjacent level versus respecting the native angle or fixating in lordosis. These findings may provide a biomechanical basis for failures that are often observed with the inadequate restoration of segmental lordosis after lumbar fusion. Spine surgeons who are not acquainted with spinal deformity correction concepts and who usually perform only monosegment or short-segment lumbar fusion should also consider these findings during surgical planning.

Acknowledgments

We thank the staff of Neuroscience Publications at Barrow Neurological Institute for assistance with manuscript preparation.

Disclosures

Dr. Turner: consultant for NuVasive, SeaSpine, and Alphatec Spine. Dr. Uribe: consultant for NuVasive, SI-BONE, Misonix, Mainstay, and Viseon. Ms. Lehrman: employee of Stryker at the time of submission.

Author Contributions

Conception and design: Turner, de Andrada Pereira, Kelly. Acquisition of data: de Andrada Pereira, Wangsawatwong, Sawa, O’Neill. Analysis and interpretation of data: Turner, de Andrada Pereira, Lehrman, Sawa, Godzik, Kelly. Drafting the article: de Andrada Pereira, Wangsawatwong. Critically revising the article: de Andrada Pereira, Wangsawatwong, Farber. Reviewed submitted version of manuscript: Turner, de Andrada Pereira, Kelly. Statistical analysis: Lehrman, Sawa. Administrative/technical/material support: Turner, Kelly. Study supervision: Turner, Uribe, Kelly.

References

  • 1

    Glassman SD, Berven S, Bridwell K, Horton W, Dimar JR. Correlation of radiographic parameters and clinical symptoms in adult scoliosis. Spine (Phila Pa 1976). 2005;30(6):682688.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Roussouly P, Pinheiro-Franco JL. Biomechanical analysis of the spino-pelvic organization and adaptation in pathology. Eur Spine J. 2011;20(suppl 5):609618.

  • 3

    Roussouly P, Gollogly S, Berthonnaud E, Dimnet J. Classification of the normal variation in the sagittal alignment of the human lumbar spine and pelvis in the standing position. Spine (Phila Pa 1976). 2005;30(3):346353.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Le Huec JC, Aunoble S, Philippe L, Nicolas P. Pelvic parameters: origin and significance. Eur Spine J. 2011;20(suppl 5):564571.

  • 5

    Le Huec JC, Charosky S, Barrey C, Rigal J, Aunoble S. Sagittal imbalance cascade for simple degenerative spine and consequences: algorithm of decision for appropriate treatment. Eur Spine J. 2011;20(suppl 5):699703.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Vaz G, Roussouly P, Berthonnaud E, Dimnet J. Sagittal morphology and equilibrium of pelvis and spine. Eur Spine J. 2002;11(1):8087.

  • 7

    Bae JS, Lee SH, Kim JS, Jung B, Choi G. Adjacent segment degeneration after lumbar interbody fusion with percutaneous pedicle screw fixation for adult low-grade isthmic spondylolisthesis: minimum 3 years of follow-up. Neurosurgery. 2010;67(6):16001608.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Djurasovic MO, Carreon LY, Glassman SD, Dimar JR II, Puno RM, Johnson JR. Sagittal alignment as a risk factor for adjacent level degeneration: a case-control study. Orthopedics. 2008;31(6):546.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Park MS, Kelly MP, Lee DH, Min WK, Rahman RK, Riew KD. Sagittal alignment as a predictor of clinical adjacent segment pathology requiring surgery after anterior cervical arthrodesis. Spine J. 2014;14(7):12281234.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Phan K, Nazareth A, Hussain AK, et al. Relationship between sagittal balance and adjacent segment disease in surgical treatment of degenerative lumbar spine disease: meta-analysis and implications for choice of fusion technique. Eur Spine J. 2018;27(8):19811991.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Zheng G, Wang C, Wang T, et al. Relationship between postoperative lordosis distribution index and adjacent segment disease following L4-S1 posterior lumbar interbody fusion. J Orthop Surg Res. 2020;15(1):129.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Yee TJ, Joseph JR, Terman SW, Park P. Expandable vs static cages in transforaminal lumbar interbody fusion: Radiographic comparison of segmental and lumbar sagittal angles. Neurosurgery. 2017;81(1):6974.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Cheng X, Zhang F, Zhang K, et al. Effect of single-level transforaminal lumbar interbody fusion on segmental and overall lumbar lordosis in patients with lumbar degenerative disease. World Neurosurg. 2018;109:e244e251.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Saadeh YS, Joseph JR, Smith BW, Kirsch MJ, Sabbagh AM, Park P. Comparison of segmental lordosis and global spinopelvic alignment after single-level lateral lumbar interbody fusion or transforaminal lumbar interbody fusion. World Neurosurg. 2019;126:e1374e1378.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Uribe JS, Myhre SL, Youssef JA. Preservation or restoration of segmental and regional spinal lordosis using minimally invasive interbody fusion techniques in degenerative lumbar conditions: a literature review. Spine (Phila Pa 1976). 2016;41(suppl 8):S50S58.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Miyazaki M, Ishihara T, Abe T, et al. Effect of intraoperative position in single-level transforaminal lumbar interbody fusion at the L4/5 level on segmental and overall lumbar lordosis in patients with lumbar degenerative disease. Medicine (Baltimore). 2019;98(39):e17316.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Lovecchio FC, Vaishnav AS, Steinhaus ME, et al. Does interbody cage lordosis impact actual segmental lordosis achieved in minimally invasive lumbar spine fusion?. Neurosurg Focus. 2020;49(3):E17.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Panjabi MM. Biomechanical evaluation of spinal fixation devices: I. A conceptual framework. Spine (Phila Pa 1976). 1988;13(10):11291134.

  • 19

    Kelly BP, Bennett CR. Design and validation of a novel Cartesian biomechanical testing system with coordinated 6DOF real-time load control: application to the lumbar spine (L1-S, L4-L5). J Biomech. 2013;46(11):19481954.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Crawford NR, Dickman CA. Construction of local vertebral coordinate systems using a digitizing probe. Technical note. Spine (Phila Pa 1976). 1997;22(5):559563.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Crawford NR, Yamaguchi GT, Dickman CA. A new technique for determining 3-D joint angles: the tilt/twist method. Clin Biomech. (Bristol, Avon). 1999;14(3):153165.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Potter BK, Lenke LG, Kuklo TR. Prevention and management of iatrogenic flatback deformity. J Bone Joint Surg Am. 2004;86(8):17931808.

  • 23

    Kettler A, Wilke HJ, Haid C, Claes L. Effects of specimen length on the monosegmental motion behavior of the lumbar spine. Spine (Phila Pa 1976). 2000;25(5):543550.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Dickey JP, Kerr DJ. Effect of specimen length: are the mechanics of individual motion segments comparable in functional spinal units and multisegment specimens?. Med Eng Phys. 2003;25(3):221227.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Ruspi ML, Palanca M, Faldini C, Cristofolini L. Full-field in vitro investigation of hard and soft tissue strain in the spine by means of Digital Image Correlation. Muscles Ligaments Tendons J. 2018;7(4):538545.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Gustafson H, Siegmund G, Cripton P. Comparison of strain rosettes and digital image correlation for measuring vertebral body strain. J Biomech Eng. 2016;138(5):054501.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Palanca M, Brugo TM, Cristofolini L. Use of digital image correlation to investigate the biomechanics of the vertebra. J Mech Med Biol. 2015;15(02):1540004.

  • 28

    Oda I, Cunningham BW, Buckley RA, et al. Does spinal kyphotic deformity influence the biomechanical characteristics of the adjacent motion segments? An in vivo animal model. Spine (Phila Pa 1976). 1999;24(20):21392146.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Menezes-Reis R, Bonugli GP, Dalto VF, da Silva Herrero CFP, Defino HLA, Nogueira-Barbosa MH. Association between lumbar spine sagittal alignment and l4-l5 disc degeneration among asymptomatic young adults. Spine (Phila Pa 1976). 2016;41(18):E1081E1087.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Zhao X, Du L, Xie Y, Zhao J. Effect of lumbar lordosis on the adjacent segment in transforaminal lumbar interbody fusion: a finite element analysis. World Neurosurg. 2018;114:e114e120.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Umehara S, Zindrick MR, Patwardhan AG, et al. The biomechanical effect of postoperative hypolordosis in instrumented lumbar fusion on instrumented and adjacent spinal segments. Spine (Phila Pa 1976). 2000;25(13):16171624.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Molz FJ, Kirkpatrick JS, Reza Moeini SM, Partin JI, Bidez MW. Effects of kyphosis and lordosis on the remaining lumbar vertebral levels within a thoracolumbar fusion: an experimental study of the multisegmental human spine. J South Orthop Assoc. 1999;8(4):261268.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand

Images from de Andrada Pereira et al. (pp 525–534).

  • FIG. 1.

    Lateral radiographs showing the L4–5 pedicle screw and rod instrumentation and conditions tested. A: Lordosis condition: 5° of lordosis added to the natural segmental angle, using the compressor tool on the bilateral pedicle screw tulip heads, resulting in 18° segmental lordosis. B: Neutral condition: natural segmental angle of 13°. C: Kyphosis condition: 5° of kyphosis added to the natural segmental angle, using the distractor tool on the bilateral pedicle screw tulip heads, resulting in 8° segmental kyphosis. Figure is available in color online only.

  • FIG. 2.

    DIC layout and examples. A: Superior view of the layout for the DIC camera (left lateral) and Optotrak camera (right lateral) relative to the vertebral specimen. B: Photograph of a specimen mounted to a robotic test frame depicting the speckle pattern applied to soft tissue and bone on the anterior spinal column. C: Computer screenshot of analyzed speckle pattern using DIC software showing maximum principal strain distribution during the pure moment flexion test. Figure is available in color online only.

  • FIG. 3.

    Intervertebral disc subregions of interest (anteroposterior quarters). Figure is available in color online only.

  • FIG. 4.

    A and B: Illustrations representing models with different index-level angles (white lines) with 5° of lordosis (A) and 5° of kyphosis (B) from the native angle. The yellow boxes represent the adjacent-segment discs, where the DIC analyses were performed. C and D: DIC camera analysis of the adjacent-segment disc with different index-level angles in lordosis (C) and kyphosis (D) for a single-level L4–5 pedicle screw and rod fusion. Panels 4A and 4B used with permission from Barrow Neurological Institute, Phoenix, Arizona. Figure is available in color online only.

  • FIG. 5.

    Mean (SD) ROM for all load directions at L3–4, the superior adjacent level to instrumentation. #Statistically significant difference compared with kyphosis condition (p < 0.05). *Statistically significant difference compared with neutral condition (p < 0.05). C = compression; EX = extension; FL = flexion; LAR = left axial rotation; LLB = left lateral bending; RAR = right axial rotation; RLB = right lateral bending.

  • FIG. 6.

    Mean (SD) E1 and E2 per subregion of L3–4 disc (Q1, Q2, Q3, and Q4). #Statistically significant difference compared with lordosis condition (p < 0.05). *Statistically significant difference compared with neutral condition (p < 0.05).

  • 1

    Glassman SD, Berven S, Bridwell K, Horton W, Dimar JR. Correlation of radiographic parameters and clinical symptoms in adult scoliosis. Spine (Phila Pa 1976). 2005;30(6):682688.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Roussouly P, Pinheiro-Franco JL. Biomechanical analysis of the spino-pelvic organization and adaptation in pathology. Eur Spine J. 2011;20(suppl 5):609618.

  • 3

    Roussouly P, Gollogly S, Berthonnaud E, Dimnet J. Classification of the normal variation in the sagittal alignment of the human lumbar spine and pelvis in the standing position. Spine (Phila Pa 1976). 2005;30(3):346353.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Le Huec JC, Aunoble S, Philippe L, Nicolas P. Pelvic parameters: origin and significance. Eur Spine J. 2011;20(suppl 5):564571.

  • 5

    Le Huec JC, Charosky S, Barrey C, Rigal J, Aunoble S. Sagittal imbalance cascade for simple degenerative spine and consequences: algorithm of decision for appropriate treatment. Eur Spine J. 2011;20(suppl 5):699703.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Vaz G, Roussouly P, Berthonnaud E, Dimnet J. Sagittal morphology and equilibrium of pelvis and spine. Eur Spine J. 2002;11(1):8087.

  • 7

    Bae JS, Lee SH, Kim JS, Jung B, Choi G. Adjacent segment degeneration after lumbar interbody fusion with percutaneous pedicle screw fixation for adult low-grade isthmic spondylolisthesis: minimum 3 years of follow-up. Neurosurgery. 2010;67(6):16001608.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Djurasovic MO, Carreon LY, Glassman SD, Dimar JR II, Puno RM, Johnson JR. Sagittal alignment as a risk factor for adjacent level degeneration: a case-control study. Orthopedics. 2008;31(6):546.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Park MS, Kelly MP, Lee DH, Min WK, Rahman RK, Riew KD. Sagittal alignment as a predictor of clinical adjacent segment pathology requiring surgery after anterior cervical arthrodesis. Spine J. 2014;14(7):12281234.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Phan K, Nazareth A, Hussain AK, et al. Relationship between sagittal balance and adjacent segment disease in surgical treatment of degenerative lumbar spine disease: meta-analysis and implications for choice of fusion technique. Eur Spine J. 2018;27(8):19811991.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Zheng G, Wang C, Wang T, et al. Relationship between postoperative lordosis distribution index and adjacent segment disease following L4-S1 posterior lumbar interbody fusion. J Orthop Surg Res. 2020;15(1):129.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Yee TJ, Joseph JR, Terman SW, Park P. Expandable vs static cages in transforaminal lumbar interbody fusion: Radiographic comparison of segmental and lumbar sagittal angles. Neurosurgery. 2017;81(1):6974.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Cheng X, Zhang F, Zhang K, et al. Effect of single-level transforaminal lumbar interbody fusion on segmental and overall lumbar lordosis in patients with lumbar degenerative disease. World Neurosurg. 2018;109:e244e251.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Saadeh YS, Joseph JR, Smith BW, Kirsch MJ, Sabbagh AM, Park P. Comparison of segmental lordosis and global spinopelvic alignment after single-level lateral lumbar interbody fusion or transforaminal lumbar interbody fusion. World Neurosurg. 2019;126:e1374e1378.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Uribe JS, Myhre SL, Youssef JA. Preservation or restoration of segmental and regional spinal lordosis using minimally invasive interbody fusion techniques in degenerative lumbar conditions: a literature review. Spine (Phila Pa 1976). 2016;41(suppl 8):S50S58.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Miyazaki M, Ishihara T, Abe T, et al. Effect of intraoperative position in single-level transforaminal lumbar interbody fusion at the L4/5 level on segmental and overall lumbar lordosis in patients with lumbar degenerative disease. Medicine (Baltimore). 2019;98(39):e17316.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Lovecchio FC, Vaishnav AS, Steinhaus ME, et al. Does interbody cage lordosis impact actual segmental lordosis achieved in minimally invasive lumbar spine fusion?. Neurosurg Focus. 2020;49(3):E17.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Panjabi MM. Biomechanical evaluation of spinal fixation devices: I. A conceptual framework. Spine (Phila Pa 1976). 1988;13(10):11291134.

  • 19

    Kelly BP, Bennett CR. Design and validation of a novel Cartesian biomechanical testing system with coordinated 6DOF real-time load control: application to the lumbar spine (L1-S, L4-L5). J Biomech. 2013;46(11):19481954.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Crawford NR, Dickman CA. Construction of local vertebral coordinate systems using a digitizing probe. Technical note. Spine (Phila Pa 1976). 1997;22(5):559563.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Crawford NR, Yamaguchi GT, Dickman CA. A new technique for determining 3-D joint angles: the tilt/twist method. Clin Biomech. (Bristol, Avon). 1999;14(3):153165.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Potter BK, Lenke LG, Kuklo TR. Prevention and management of iatrogenic flatback deformity. J Bone Joint Surg Am. 2004;86(8):17931808.

  • 23

    Kettler A, Wilke HJ, Haid C, Claes L. Effects of specimen length on the monosegmental motion behavior of the lumbar spine. Spine (Phila Pa 1976). 2000;25(5):543550.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Dickey JP, Kerr DJ. Effect of specimen length: are the mechanics of individual motion segments comparable in functional spinal units and multisegment specimens?. Med Eng Phys. 2003;25(3):221227.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Ruspi ML, Palanca M, Faldini C, Cristofolini L. Full-field in vitro investigation of hard and soft tissue strain in the spine by means of Digital Image Correlation. Muscles Ligaments Tendons J. 2018;7(4):538545.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    Gustafson H, Siegmund G, Cripton P. Comparison of strain rosettes and digital image correlation for measuring vertebral body strain. J Biomech Eng. 2016;138(5):054501.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Palanca M, Brugo TM, Cristofolini L. Use of digital image correlation to investigate the biomechanics of the vertebra. J Mech Med Biol. 2015;15(02):1540004.

  • 28

    Oda I, Cunningham BW, Buckley RA, et al. Does spinal kyphotic deformity influence the biomechanical characteristics of the adjacent motion segments? An in vivo animal model. Spine (Phila Pa 1976). 1999;24(20):21392146.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Menezes-Reis R, Bonugli GP, Dalto VF, da Silva Herrero CFP, Defino HLA, Nogueira-Barbosa MH. Association between lumbar spine sagittal alignment and l4-l5 disc degeneration among asymptomatic young adults. Spine (Phila Pa 1976). 2016;41(18):E1081E1087.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Zhao X, Du L, Xie Y, Zhao J. Effect of lumbar lordosis on the adjacent segment in transforaminal lumbar interbody fusion: a finite element analysis. World Neurosurg. 2018;114:e114e120.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Umehara S, Zindrick MR, Patwardhan AG, et al. The biomechanical effect of postoperative hypolordosis in instrumented lumbar fusion on instrumented and adjacent spinal segments. Spine (Phila Pa 1976). 2000;25(13):16171624.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Molz FJ, Kirkpatrick JS, Reza Moeini SM, Partin JI, Bidez MW. Effects of kyphosis and lordosis on the remaining lumbar vertebral levels within a thoracolumbar fusion: an experimental study of the multisegmental human spine. J South Orthop Assoc. 1999;8(4):261268.

    • PubMed
    • Search Google Scholar
    • Export Citation

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