Accepted Manuscript

Effect of lumbar lordosis on the adjacent segment in transforaminal lumbar interbody

fusion: A finite element analysis

Xin Zhao, MD, Lin Du, Youzhuan Xie, MD, Jie Zhao, MD

PII: S1878-8750(18)30344-9
DOI: 10.1016/j.wneu.2018.02.073
Reference: WNEU 7488

To appear in: World Neurosurgery

Received Date: 2 November 2017

Revised Date: 9 February 2018
Accepted Date: 12 February 2018

Please cite this article as: 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 Neurosurgery
(2018), doi: 10.1016/j.wneu.2018.02.073.

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 ACCEPTED MANUSCRIPT

Effect of lumbar lordosis on the adjacent segment in transforaminal lumbar

interbody fusion: A finite element analysis

Short title: LL effects on adjacent segment in TLIF

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Xin Zhao1, MD, Lin Du1, Youzhuan Xie1, MD and Jie Zhao1*, MD

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Department of Orthopaedic Surgery, Shanghai Ninth People's Hospital, Shanghai

Jiaotong University School of Medicine, Shanghai, China

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Shanghai Key Laboratory of Orthopaedic Implants，Department of Orthopaedic

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Surgery, Shanghai Ninth People's Hospital, Shanghai Jiao Tong University School
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of Medicine

*Corresponding Author
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Jie Zhao
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Shanghai Ninth People's Hospital, Shanghai Jiaotong University School of Medicine,

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Discipline Construction Research Center of China Hospital Development Institute,

Shanghai Jiao Tong University, 639 Zhizaoju Road, Shanghai 200011, People’s
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Republic of China
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Telephone: +86-21-23271159
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Fax: +86-21-63139920

E-mail: profzhaojie@sina.com
 Xin Zhao 1
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Abstract

Objective: Here we used a finite element (FE) analysis to investigate the

biomechanical changes caused by transforaminal lumbar interbody fusion (TLIF) at

the L4-L5 level by lumbar lordosis (LL) degree.

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Methods: A lumbar FE model (L1-S5) was constructed based on computed

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tomography scans of a 30-year-old healthy male volunteer (pelvic incidence = 50°, LL

= 52°). We investigated the influence of LL on the biomechanical behavior of the

SC
lumbar spine after TLIF in L4-L5 fusion models with 57°, 52°, 47°, and 40° LL. The

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LL was defined as the angle between the superior endplate of L1 and the superior
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endplate of S1. A 150-N vertical axial pre-load was imposed on the superior surface

of L3. A 10-N·m moment was simultaneously applied on the L3 superior surface

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along the radial direction to simulate the four basic physiological motions of flexion,
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extension, lateral bending, and torsion in the numerical simulations. The range of
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motion (ROM) and intradiscal pressure (IDP) of L3-L4 were evaluated and compared

in the simulated cases.

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Results: In all motion patterns, the ROM and IDP were both increased after TLIF. In
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addition, the decrease in lordosis generally increased the ROM and IDP in all motion
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patterns.

Conclusions: The current FE analysis indicated that decreased spinal lordosis may

evoke overstress of the adjacent segment and increase the risk of the pathological

development of adjacent segment degeneration (ASD); thus, ASD should be

considered when planning a spinal fusion procedure.

 Xin Zhao 2
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Key words: Adjacent segment degeneration; Transforaminal lumbar interbody fusion;

Lumbar lordosis; Range of motion; Intradiscal pressure

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Introduction

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Transforaminal lumbar interbody fusion (TLIF) is a common surgical treatment for

degenerative lumbar diseases. However, spinal fusion may cause biomechanical

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changes, such as increased motion and mechanical stress at the adjacent segment,

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resulting in pathologies such as accelerated degeneration (1, 2). Radiographic and
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clinical degeneration in the adjacent segment was reportedly detected in 43% and 24%

of patients after TLIF, respectively (3). In some cases, degeneration of the adjacent
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segments may cause significant symptoms that require revision surgery. Therefore,
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increasing our understanding the pathology and prevention of adjacent segment

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pathologies is of great clinical importance.

Sagittal shape is highly important in spinal physiology and pathophysiology. Pelvic

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and spinal positional parameters are important characteristics correlated with spinal
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physiology and pathophysiology. It has been suggested that the sagittal alignment of
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the spine and pelvis may influence the development of adjacent segment degeneration

(ASD). Abnormal sagittal alignment after spinal fusion is thought to be a cause of

biomechanical alteration and ASD (4). “Pelvic incidence (PI),” defined as the angle

between the line perpendicular to the sacral plate at its midpoint and the line

connecting this point to the axes of the femoral heads, is the most consistent
 Xin Zhao 3
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parameter strongly correlated with various pelvic and spinal positional parameters and

is a useful predictor of lordosis. Boulay et al (5) demonstrated an equation for

predicting lumbar lordosis (LL) based on PI. If the adaptation potential of the spine

and pelvis exceeds the value as per the equation, it may evoke pathological positions

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and loading patterns, which also may be relevant to the development of ASD. In

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Dominique’ study, a relationship between PI–LL (PILL) mismatch as a measure for

spinopelvic alignment and the risk of ASD was established; the results showed that a

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high PI with diminished LL seems to predispose an individual to ASD (6).

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Since biomechanical changes are responsible for the pathology of ASD after lumbar

fusion, biomechanical studies such as finite element (FE) analysis has been often used
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to understand the changes in motion and stress at adjacent segments after spinal
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fusion, as well as their potential effects on the pathology of ASD (7, 8). Many
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morphological and positional parameters have been investigated to determine their

correlation with the development of ASD. Here we developed an FE model to

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investigate the biomechanical changes resulting from the TLIF models with different
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LL degrees to determine the influence of a PILL mismatch on ASD after TLIF at the
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L4-L5 level.

Materials and methods

Lumbar FE model (L1-S5)

A surface model including the L1-S5 segment was first constructed based on
 Xin Zhao 4
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computed tomography scan images of a 30-year-old healthy male volunteer (SS = 42°,

PI = 50°, LL = 52°). A corresponding solid model was then constructed using

Hypermesh (Altair Engineering, USA). After the meshing was implemented, a

biomechanical FE analysis of the L1-S1 segment was performed using

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ABAQUS/Explicit.

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The model included the vertebrae, intervertebral discs, endplates, and ligaments. As

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shown in Fig. 1, the vertebrae were divided into cortical and cancellous bones

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represented by an outer layer of hexahedral solid elements and enclosed tetrahedral
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solid elements, respectively. The thickness of the cortical bones was assumed to be 1

mm according to a previous study(9). The nodes were shared at the interface between
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the cortical and cancellous bones to avoid a complex interaction. Bones usually render
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a highly non-linear biomechanical response under large loading conditions such as

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impact and bone fracture (10). In the current study, since we focused on the

biomechanical behavior of the lumbar spine under daily physiological motion, the
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cortical and cancellous bones were assumed to be homogeneous and isotropic

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materials with different elastic constants as listed in Table 1 (11). Contact surfaces
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with a distance of 0.5 mm were defined to simulate the facet joints (12).

The intervertebral discs were divided into superior and inferior endplates, annulus

fibrosus, and nucleus pulposus. The endplates had a thickness of 0.5 mm (13) and

were connected to the adjacent vertebrae by sharing common nodes on the interfaces.
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They were meshed by 3D solid elements and assigned to a linear isotropic elastic

model with material parameters as listed in Table 1. An estimated 30–50% of the

cross-sectional area of the disc was defined as the nucleus, while the rest was

processed as the annulus fibrosus. The nucleus is assumed to be a nearly

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incompressible material with a Poisson’s ratio of 0.499 and a low Young's modulus of

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1 MPa. The ROM of the human spine is mainly affected by the intervertebral discs.

The rationality of the constitutive model for large deformation segments such as

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annulus fibrosus was considered to obtain accurate results. The annulus fibrosus was

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often characterized as fiber-reinforced materials in which several matrix layers are
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embedded with rebar elements representing collagen fibers (14-16). The effect of the

interaction between the fibers and the matrix was ignored when using the
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one-dimensional rebar elements method. At the same time, this method increases
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meshing difficulty. To overcome these shortcomings, Peng et al. (17) developed a

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continuum mechanics–based fiber-reinforced hyperelastic model to characterize the

anisotropic nonlinear biomechanical behavior of the annulus fibrosus. The stain

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energy function used to determine the constitutive relationship was given as follows:
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W = WM + WF + WFM
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where WM, WF, and WFM are the energy contribution from the ground matrix, fiber

elongation, and matrix–fiber interaction, respectively. The specific forms of strain

energy functions for the annulus fibrosis are given as follows:

1

 =  ̅ − 3 +  − 1

0  ≤ 1

 =  
  − 1 +   − 1  > 1
 
 Xin Zhao 6
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=
  ,  =    =     −   +   − 1

!
where   = ,/ 0 = 1, … ,5 are principal invariants and C10 =
"#$%&'()*+ '*∗+ -.

0.034(MPa), D1 = 0.197(MPa-1), C2 = 0.45(MPa), C3 = 82.6(MPa), 3 = 12.0MPa

9 = 125, and :∗ = 1.02 are material parameters. This constitutive model was

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implemented by designing a user-defined material subroutine (UANISOHYPER) in

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ABAQUS/Standard. Fiber orientation was defined as ±30° to the horizontal plane

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(17-18).

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Ligaments play a major role in spinal stability and function. Five ligaments including
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the anterior longitudinal ligament (ALL), posterior longitudinal ligament (PLL),
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ligamentum flavum (LF), interspinous ligament (ISL), and supraspinal ligament (SSL)

were modeled as isotropic linear elastic membranes that can bear tensile loads only.
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The material parameters for different parts of the model are summarized in Table 1.
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TLIF of L4-L5 models with different LL degrees

The TLIF model was constructed by removing the right L4 lamina, facet joint, and LF
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while preserving the spinous process, contralateral lamina, and facet joint as well as

the left LF, SSL, and ISL. Posterior bilateral pedicle screw fixation was performed in

the L4 and L5 vertebrae. The cage was inserted into the L4-L5 intervertebral space to

simulate fusion.

All screws had a sharp thread to prevent relative motion at the bone–screw interface.
 Xin Zhao 7
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Except for the screw tip, the surface of the screw was fixed to the bone without

allowing relative motion. A ‘‘tie’’ contact condition was used to enable permanent

binding between screw threads and vertebrae by full constraint. The diameter of each

pedicle screw was assumed to be 5.0 mm, and the mean outer diameter (including

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thread height) of the real screws was 6.5 mm. The length of the screws was 40 mm.

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The screws were inserted into the pedicles of L4 and L5. The screws were inserted

horizontally, with an inward incline of 10°. The rods were 5.5 mm in diameter. All

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instruments were made of titanium alloy (Ti6Al4V).

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In the intervertebral fusion procedure, the entire nucleus and part of the annulus at the

posterior right side were removed. The anterior aspect of the disc space was
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asymmetrically inserted with a single polyetheretherketone Z-cage (WeGo company,

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Shandong, China) diagonally positioned at 45° in the middle and posterior disc space.
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The cage was filled with cancellous bone to simulate the embedded bone graft within

the implanted cage. The cage–bone interface was modeled by surface-to-surface

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contact elements to simulate the early postoperative stage after the TLIF surgeries.
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The coefficient of friction at the cage–vertebra interface was 0.2 to mimic small teeth
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on the contact surfaces (19). The properties of the screw and cage materials are listed

in Table 2.

To investigate the influence of LL on the biomechanical behavior of the lumbar spine

after TLIF, the L1-S5 segment with L4-L5 fusion models was modified to different
 Xin Zhao 8
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LL degrees. LL was defined as the angle between the superior endplate of L1 and the

superior endplate of S1. The change of the LL resulted from the change of the

segmental LL of L4-L5, which received intervertebral fusion at different sagittal

angles. Then, according to PILL > 10° as the PILL mismatch criterion (6) and the

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parameter of the lumbar model of the volunteer (PI = 50°, LL = 52°), four L4-L5

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fusion models were constructed: 57°, 52°, 47°, and 40° (Fig. 1).

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Boundary and loading conditions

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Considering the human spine’s daily physiological actions, four basic motions
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including flexion, extension, lateral bending, and torsion were selected in the

numerical simulations. The biomechanical characteristics of the adjacent segment

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level were investigated in the FE models of the lumbar spine (L3-L5). L5 was
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completely constrained. According to Yamamoto’s study (20), a 150-N vertical axial

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pre-load was imposed on the superior surface of L3. A 10-N·m moment was applied

on the L3 superior surface along the radial direction at the same time to simulate the
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four basic physiological motions. The ranges of motion (ROMs) and intradiscal
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pressures (IDPs) of L3-L4 were calculated and compared among the simulated cases.
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Model validation

For model validation, ROMs under the different human physiological motions were

employed as verification criteria. The L3-L5 intact model with an LL= 52° was

investigated. ROMs of the L3-L4 level under flexion, extension, lateral bending, and
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torsion with a 150-N pre-load and a 10-N·m moment were measured. ROMs reported

by different research groups (20, 21) were compared (Table 3). Then, numerical

simulations were extended to other L3-L5 models with L4-L5 intervertebral fusion of

different LL.

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Results

The biomechanical characteristics of the adjacent L3–L4 segment was compared in

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the FE models of four L4-L5 fusion models with four LL angles (57°, 52°, 47°, and

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40°) and the original model (without fusion, LL = 52°) in the four basic physiological
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motions (flexion, extension, lateral bending, and torsion). As shown in Fig. 2 and

Table 4, in all motion patterns, TLIF increased both the ROM and the IDP compared
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to those in the original model. In addition, a decrease in lordosis degree generally

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increased the ROMs and IDPs of all motion patterns.

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Discussion
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ASD after TLIF are among the most important sequelae affecting the long-term
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results. To the best of our knowledge, the present study is the first to analyze the
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influence of LL (PILL mismatch versus match) on the biomechanical characteristics

of the adjacent segment after L4-L5 TLIF using FE analysis. The results showed that

as LL decreased, the stress of the adjacent disc increased.

In our previous domestic studies, the effects of sagittal fixation angle on adjacent
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segment stress in lumbar fusion were analyzed in a human cadaver. The results

showed that spinal fixation can increase stress within the adjacent segments. Lumbar

fixation with abnormal sagittal angles may further deteriorate the associated

biomechanical conditions. However, each cadaver has an inherent anatomical and

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biomechanical profile, including not only LL but also other parts of each vertebra and

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disc. FE modeling allows one to parametrically alter a single input factor such as LL

geography at a given point in time and analyze the biomechanical results. In the

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current study, we used validated FE models of the lumbar spine that had different LL

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degrees but otherwise identical geographic patterns and biomechanical properties. The
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results showed that abnormal sagittal angles may further deteriorate the associated

biomechanical condition.
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In a previous study (22) of two patients grouped by the threshold of △PILL > 15°,
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subjects with a greater PILL mismatch exhibit higher shear stresses before and after

simulated fusion, which may account for the clinically observed ASD after lumbar
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fusion. In the musculoskeletal simulation adopted in this study, shear stress and
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compression stress were obtained using the force decomposition method, which could
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only indicate the two-dimensional stress distribution of the sagittal plane. In our study,

the FE analysis method was used to investigate the biomechanical characteristics of

the adjacent segment; the stress distribution in the three-dimensional condition is

characterized by von Mises stress. These results further demonstrated the influence of

sagittal angle on the stress and ROM of the adjacent segments in spinal fusion.
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Sagittal balance is among the most reliable factors that influence ASD development.

LL is a critical feature of spinal morphology that is correlated with different

pathological conditions. Risk factor studies in the clinical setting have suggested that

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lordosis might be correlated with ASD development (23, 24). Fusion procedures may

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result in small lordotic changes. However, lordosis can frequently be restored after the

procedure. In clinical study settings, hypolordosis may increase the risk of adjacent

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segment deterioration (25-27).

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Since the various positioning and inclusion of the spinal segment can cause significate

measurement variation and demographic characteristics and physical activities can

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affect the results of a lordosis test, consensus about the normal range of LL is lacking.
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PI is suggested to be the most consistent parameter in close correlation with lordosis

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prediction (17). Although increased PI was among the suggested potential risk factors

for ASD, it correlation with ASD was not consistently observed. It has been suggested
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that although PI indirectly reflects the overall sagittal balance, it alone does not
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predispose one to the risk of imbalance and ASD. Instead, the PILL mismatch after
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lumbar spinal fusion was suggested to predispose patients to ASD (18, 22).

The current study investigated the influence of LL on ASD in an FE model with a

fixed PI of 50°. The LL degrees in the study models were set according to the

threshold of PILL > 10° as PILL mismatch criteria (18). However, since the lumbar
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semicircular was removed to preserve the lumbar fusion model of the contralateral

articular facet, when the LL was set > 57°, the rear articular facet would collide with

the joint. Therefore, the upper limit of LL was set at 57°, this limited our conclusion

about whether more significant lordosis would cause different ROM and IDT changes;

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thus, this question must be addressed further in future studies. Another limitation of

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the model is that it does not consider the effect of so-called compensatory

mechanisms. If a cage with a certain lordosis is implanted at L4-L5, some kyphotic

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compensatory changes will occur in the adjacent segment. As calculating the

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compensatory changes that occur in the adjacent segment was very complex, we had
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to define the angle of the entire LL instead of the angle of the segment’s LL in the

model. Therefore, we did not take into this account when establishing the TLIF EF
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model.
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In conclusion, the current FE analysis indicated that a decreased spinal lordosis may

evoke overstress of the adjacent segment and predispose a patient to an increased risk
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of the pathological development of ASD; therefore, it should be considered in the

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planning of spinal fusion procedures.

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Funding

This research did not receive any specific grant from funding agencies in the public,

commercial, or not-for-profit sectors.

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Conflicts of interest

None

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Figure legends
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Fig. 1. L4-L5 lumbar fusion models with different lordosis degrees.

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Fig. 2. The intradiscal pressure (IDP) and range of motion (ROM) at L3-L4 in the

fusion original (without fusion) and fusion models with different lordosis degrees.
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Table 1 Properties of materials in finite analysis

Material Young's Poisson's ratio Element References

modulus E ν type

(MPa)

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Vertebrae

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Cortical bone 12000 0.3 C3D8 (11,12)

Cancellous 100 0.2 C3D4 (11,12)

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bone

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Endplate 12000 0.3 C3D8 (21)
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Disc

Nucleus 1 0.499 C3D8 (21)

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Annulus User Material C3D8 (17)

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fibrosus defined
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Ligaments

ALL 7.8 0.3 S4 (21)

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PLL 10 0.3 S4 (21)

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LF 15 0.3 S4 (21)
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CL 7.5 0.3 S4 (21)

ISL 8 0.3 S4 (21)

SSL 8 0.3 S4 (21)

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Table 2 Material properties used in finite element model of lumbar fusion

systems

Material Young’s modulus Poisson’s ratio

PEEK 3.6 GPa 0.3

PT
Ti6A17Nb 114 GPa 0.3

RI
Ti6A14V 114 GPa 0.3

U SC
AN
M
D
TE
C EP
AC
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Table 3 Range of Motions (ROMs, degree) of L3-L4 in different motions from

different studies

Studies Flexion Extension Lateral Torsion

bending

PT
Chen (21) 3.58 1.18 3.33 2.21

RI
Yamamoto (20) 6.1 2.3 4.3 4

Present study 4.48 2.46 3.9 4.48

U SC
AN
M
D
TE
C EP
AC
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Table 4 The influence of lumbar fusion and lordosis on intradiscal pressure (IDP)

and range of motion (ROM) of L3-L4 segments

Flexion Extension Lateral bending Torsion

PT
LL=40° IDP (Mpa) 0.94 0.81 1.03 0.97

RI
ROM (degree) 6.39 4.68 5.25 3.51

LL=47° IDP (Mpa) 0.82 0.77 0.94 0.81

SC
ROM (degree) 5.735 4.37 4.64 3.17

U
LL=52° IDP (Mpa) 0.73 0.74 0.83 0.67
AN
ROM (degree) 4.85 4.17 4.45 2.89

LL=57° IDP (Mpa) 0.64 0.71 0.71 0.55

M

ROM (degree) 3.89 3.96 3.95 2.35

D

W/O Fusion IDP (Mpa) 0.58 0.63 0.58 0.51

TE

(LL=52°) ROM (degree) 4.4 2.4 3.9 2.4

C EP
AC
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PT
RI
U SC
AN
M
D
TE
EP
C
AC
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PT
RI
U SC
AN
M
D
TE
EP
C
AC
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Lumbar finite element models of L4-L5 fusion with four LL angles were constructed.
The results showed that a decreased spinal lordosis may evoke the overstress of the
adjacent segment. It points out that pelvic incidence–lumbar lordosis mismatch is a
risk of the pathological development of adjacent segment degeneration, which may be
considered in the planning of spinal fusion procedure.

PT
RI
U SC
AN
M
D
TE
C EP
AC
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Abbreviations

TLIF = transforaminal lumbar interbody fusion

CT = computed tomography

LL = lumbar lordosis

PT
ROM = motion

RI
ROMs = motions

IDP = intradiscal pressure

SC
FE = finite element

U
ASD = adjacent segment degeneration
AN
PILL = pelvic incidence–lumbar lordosis

ALL = longitudinal ligament

M

PLL = posterior longitudinal ligament

D

LF = ligamentum flavum
TE

ISL = interspinous ligament

SSL = supraspinal ligament

EP

PEEK = polyetheretherketone
C
AC