SPINE Volume 43, Number 18, pp E1053–E1060

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BIOMECHANICS

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Sex Specific Sacroiliac Joint Biomechanics DuringStanding Upright

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Spine

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A Finite Element Study

Amin Joukar, MS,� Anoli Shah, MS,� Ali Kiapour, PhD,� Ardalan Seyed Vosoughi, MS,� Bradley Duhon, MD,y

Anand K. Agarwal, MD,� Hossein Elgafy, MD,� Nabil Ebraheim, MD,� and Vijay K. Goel, PhD�

on the female model compared with the male model. Female

Study Design. The comparison of sacroiliac joint (SIJ) angular

motions, pelvis ligaments strain, load sharing, and stress distribu-

tion across the joint for male and female spine-pelvis-femur

models using finite element analysis.Objective. To quantify biomechanical parameters at SIJ for all

motions for both male and female models.Summary of Background Data. SIJ has been recognized as a

main source of pain in 13% to 30% of patients with low back

pain. It is shown that the SIJ rotation and translation in different

planes are not exceeding 28 to 38 and 2 mm, respectively. Due

to limitation of in vivo and in vitro studies, it is difficult to

quantify certain biomechanical parameters such as load-sharing

and stress distribution across the joint. Finite element analysis is

a useful tool which can be utilized to understand the biome-

chanics of the SIJ.Methods. The validated finite element models of a male and a

female lumbar spine-pelvis-femur were developed from com-

puter tomography (CT) scans. The models were used to simulate

spine physiological motions. The range of motion, ligament

strains, load sharing, and stress distribution across the left and

right SIJs were compared between male and female models.Results. Motions data at SIJs demonstrated that female model

experienced 86% higher mobility in flexion, 264% in extension,

143% in left bending, and 228% in right bending compared

with the male model. The stresses and loads on SIJs were higher

the �Engineering Center for Orthopaedic Research ExcellenceRE), University of Toledo, Toledo, Ohio; and ySchool of Medicine,rsity of Colorado, Denver, Colorado.

wledgment date: October 27, 2017. Acceptance date: February 21,

anuscript submitted does not contain information about medical(s)/drug(s).

ork was supported in part by NSF Industry/University Cooperativerch Center at The University of California at San Francisco, CA andniversity of Toledo, Toledo, OH (www.nsfcdmi.org).

nt financial activities outside the submitted work: consultancy,, stocks.

ss correspondence and reprint requests to Vijay K. Goel, PhD, 5046S 303, College of Engineering, University of Toledo, Toledo, OH; E-mail: Vijay.Goel@utoledo.edu

10.1097/BRS.0000000000002623

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model ligaments underwent larger strains compared with the

male model ligaments.Conclusion. Female SIJ had higher mobility, stresses, loads,

and pelvis ligament strains compared with the male SIJ which

led to higher stress across the joint, especially on the sacrum

under identical loading conditions. This could be a possible

reason for higher incidence of SIJ pain and pelvic stress fracture

in females.Key words: biomechanics, difference, female, finite elementanalysis, male, sacroiliac joint.Level of Evidence: N/A.Spine 2018;43:E1053–E1060

Low back pain (LBP) is one of the most commonreasons for primary care visits after the commoncold, with approximately 90% of adults being

impacted by this condition at some time in their lives.1,2

One of the most overlooked sources of LBP is the sacroiliacjoint (SIJ) due to its complex nature and the fact that thepain emanating from this region can mimic other hip andspine conditions.1,3 However, recent studies have reported ahigher prevalence of the SIJ as a source of LBP leadingphysicians to place greater focus on the treatment andconsideration of SIJ dysfunction as a pain generator.4

The SIJ, the largest axial joint in the body, is the articu-lation of the spine with the pelvis that allows the transfer ofloads to pelvis and lower extremities.5,6 Sexual dimorphismexists in pelvis such that compared with the male sacrum,the female sacrum is generally wider, more uneven, lesscurved, and more backward tilted. Males tend to have arelatively long and narrow pelvis, with a longer and moreconical pelvic cavity than those of females.7

There are different methods to measure the SIJ motionsuch as roentgen stereophotogrammetric, radio-stereomet-ric, and ultrasound.8–11 Using these methods, it is shownthat the SIJ rotation and translation in different planes arenot exceeding 28 to 38 and 2 mm, respectively.12,13 To theauthors’ best knowledge, there is no study which discussesthe biomechanical differences between male and female SIJs

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BIOMECHANICS Sex Specific SIJ Biomechanics During Standing Upright � Joukar et al

in terms of range of motion (ROM), SIJ ligaments strain,stress, and load sharing across the SIJ. Cadaver studieswould be technically demanding due to low motions atSIJ. In addition, quantifying stresses across the joint isnot feasible. Therefore, experimentally validated finite ele-ment analysis approach would be the most practical tool toassess the ROM, stresses, and strains across the joint. Theobjective of this study was to quantify these parameters atthe SIJ using sex specific finite element models of SIJ. Thestudy was aimed to better understand the biomechanicaldifferences in SIJ between sexes in terms of their mobilityand the possible pain sites.

MATERIAL AND METHODS

Male Finite Element Model of the Lumbar Spine-Pelvis-FemurThe previously developed and validated finite element lum-bar spine model14,15 was used for the male model. The 3-dimensional (3D) pelvis geometry was generated using a1 mm slice of computer tomography (CT) of a 55-year-oldmale pelvis without any abnormalities, degeneration, ordeformation of the pelvis. The 3D reconstruction ofspine-pelvis model was done using MIMICS software(Materialise Inc., Leuven, Belgium). After 3D reconstruc-tion of the bones and spinal discs, they were imported intoGeomagic Studio software (Raindrop Geomagic Inc., NC)to reduce noises, remove spikes, smooth surfaces, and createpatches and grids for meshing. Hypermesh software (AltairEngineering Inc., MI) was used to create the mesh structurefrom the 3D model.

Lumbar spine and pelvis bones were modeled as trabec-ular cores surrounded by a cortical layer with a thickness of1 mm.15,16 The linear hexahedral element type was utilizedfor cortical and cancellous bones of vertebrae and interver-tebral discs. Tetrahedral element type was used for thecortical and cancellous bones of the pelvis. The truss ele-ments were employed for ligamentous tissues including the

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SIJ and spinal ligaments. One lakh forty four thousand andthree hundred sixty elements were generated for the malemodel.

Female Finite Element Model of the Lumbar Spine-Pelvis-FemurCT images of a 55 years old female’s spine-pelvis withoutany abnormalities, degeneration were used to reconstructthe female spine-pelvis model. MIMICS software (Materi-alise, Leuven, Belgium) was utilized to build the 3D geome-try of the bones and then intervertebral discs were made byfilling the space between each two vertebrae of the CTimages. Next, smoothing and meshing were carried outby Geomagic Studio software (Raindrop Geomagic Inc.,NC) and the Hypermesh software (Altair Engineering, Inc.,MI). Figure 1 shows the male and female spine-pelvis-femurflexion-extension (FE) models.

The linear hexahedral element type was utilized for corti-cal bone of vertebrae and spinal discs. Tetrahedral elementswere assigned to the cancellous bone of both the vertebraeand the pelvis as well as the cortical bone of the pelvis. Thetruss elements were employed for ligamentous tissues. The SIJligaments were anterior sacroiliac ligament (ASL), inteross-eous ligament (ISL), long posterior sacroiliac ligament(LPSL), short posterior sacroiliac ligament (SPSL), sacrospi-nous ligament (SSL), and sacrotuberous ligament (STL). Adetailed view of the pelvis ligaments is shown in the Figure 2.The female model as a whole contained 463,735 elements.

Material PropertiesThe material properties used in the FE models wereextracted from previous studies14,17 for cortical and cancel-lous bones, annulus, nucleus, ligaments, and joints aresummarized in Table 1. Similar material properties wereused for both male and female models. The SIJs, spine facets,articular cartilages, and pubic symphysis were modeled asnon-linear soft contact. The femurs were kinematicallycoupled to the pelvis.

Figure 1. FE model of male spine-pelvis-femur(left), FE model of female spine-pelvis-femur(right). FE indicates flexion-extension.

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Figure 2. Anterior and posterior views ofthe pelvis finite element model. Ligamentsare demonstrated in red. (Interosseous liga-ment is not visible in this view). Anteriorview, anterior sacroiliac ligament (ASL),long posterior sacroiliac ligament (LPSL),short posterior sacroiliac ligament (SPSL),sacrospinous ligament (SSL), and sacrotu-berous ligament (STL).

BIOMECHANICS Sex Specific SIJ Biomechanics During Standing Upright � Joukar et al

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Mesh Convergence StudyThe mesh convergence analysis was done on the segregatedL4 to L5 motion segment of the female model. An initialseed size was assigned and the model was subjected to7.5 Nm bending moment to simulate motions in all planesand the ROM was measured. The mesh refining wasrepeated until the difference in the ROM in all planeswas below 4%. The final element size so determined wasused to mesh the other segments of the model. The simula-tion was run using ABAQUS 6.14 software (SIMULIA, Inc.,Providence, RI).

Finite Element Model ValidationThe intact male model SIJ ROM was previously vali-dated14,15 against study of Miller et al18 under the sameloading and posture conditions. Due to lack of data onfemale specimens SIJ ROM under two leg stance condition,the validation for the female model was performed underone leg stance condition. To be consistent, the validationunder one leg stance condition was done for both male and

TABLE 1. Material Properties of Male and Female

Component Material Properties Consti

Vertebral cortical bone E¼12,000 MPay¼0.3

Isotropic,

Vertebral cancellous bone E¼100 MPay¼0.2

Isotropic,

Pelvic cortical bone E¼17,000 MPay¼0.3

Isotropic,

Pelvic cancellous bone E¼ 10 MPay¼0.2

Isotropic,

Ground substance ofannulus fibrosis (malemodel)

C10¼0.3448D1¼0.3

Hyperelas

Ground substance ofannulus fibrosis (femalemodel)

C10¼ 0.035K1¼0.296

K2¼65

Hyperelas(HGO

Nucleus pulposus E¼1 MPay¼0.499

Isotropic,

Ligaments Nonlinear stress–straincurves

Hypoelas

Apophyseal joints – Non-linea

SIJs – Non-linea

Pubic symphysis Pressure-overclosure Non-linea

SIJ indicates sacroiliac joint.

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female models. To validate the SIJs ROM for intact maleand female models, loading conditions of the cadaver studydone by Lindsey et al19 was simulated. This experiment wascarried out for intact L4 to pelvis of the male and femalespecimens under single leg stance condition. A 7.5 Nm puremoment load was applied to the top endplate of L4 tosimulate various spinal motions. The motion at the SIJwas calculated for both right and left joints.

Loading and Boundary ConditionsIn all models, a 400 N compressive follower load wasapplied through wire elements which followed the curvatureof the lumbo-pelvis segment to simulate the effect ofmuscle forces and weight of the upper trunk. A 10 Nmbending moment was then applied at the superior surfaceof the L1 vertebrae to simulate the physiological flexion,extension, lateral bending, and axial rotation. To constrainthe models, femurs were fixed in all degrees of freedom toprevent relative displacement of the legs in two leg stancecondition.14,15

Models

tutive Relation Element Type Reference

elastic Eight nodes brick element(C3D8)

Lindsey et al14

elastic Eight nodes brick element(C3D8)

Lindsey et al14

elastic Four nodes tetrahedralelement (C3D4)

Lindsey et al14

elastic Four nodes tetrahedralelement (C3D4)

Lindsey et al14

tic, neo-Hookean Rebar Lindsey et al14

tic anisotropic)

Eight nodes brick element(C3D8)

Shahraki et al17

elastic Eight nodes brick element(C3D8)

Lindsey et al14

tic Tension-only, trusselements (T3D2)

Lindsey et al14

r soft contact – Lindsey et al14

r soft contact – Lindsey et al14

r soft contact – –

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Figure 3. Validation results for the intact female and male SIJs (right and left sides) at 7.5 Nm moment under one-leg stance condition.Experimental data were taken from Lindsey et al.19 SIJ indicates sacroiliac joint.

BIOMECHANICS Sex Specific SIJ Biomechanics During Standing Upright � Joukar et al

Data AnalysisThe SIJ motion was calculated using the angular displace-ments at the sacrum minus those at the ilium for right andleft joints. The maximum von Mises stresses, normal andshear loads across the SIJ for each of the models wereanalyzed. The average of the maximum principal strainswas calculated and Compared for all ligaments of the pelvisin the intact male and female models.

RESULTS

Model ValidationsThe predicted data for all physiological loadings fell withinone standard deviation of the experimental data, except forright lateral bending and right axial rotation for the maledata, Figure 3.

Range of MotionThe comparison of ROM at SIJ is shown in Figures 4 and 5.ROM of SIJ in the female model was the greatest in

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extension (1.368 left SIJ, 1.338 right SIJ) followed by flexion(0.508 left SIJ, 0.508 right SIJ), right rotation (0.448 left SIJ,0.448 right SIJ), right bending (0.308 left SIJ, 0.358 rightSIJ), left rotation (0.298 left SIJ, 0.338 right SIJ), and leftbending (0.248 left SIJ, 0.308 right SIJ). In the male model,the maximum ROM of SIJ occurred in left rotation (0.548left SIJ, 0.588 right SIJ) followed by right rotation (0.458 leftSIJ, 0.488 right SIJ), extension (0.378 left SIJ, 0.368 rightSIJ), flexion (0.288 left SIJ, 0.278 right SIJ), left bending(0.118 left SIJ, 0.128 right SIJ), and right bending (0.128 leftSIJ, 0.108 right SIJ). It was found that in flexion-extension(F-E) movements, SIJ had the highest motion in femalemodel (1.868), however, the male model had the greatestmotion in axial rotation (1.078). The lowest motionoccurred in lateral bending in both female and male models(0.558 vs. 0.248). According to the predicted motion datathe female model experienced 86% higher mobility inflexion, 264% in extension, 143% in left bending, and228% in right bending compared with the same motionsin the male model. In left and right rotation, the ROM of the

Figure 4. Comparison of male and femaleintact right SIJ ROM at 10 Nm momentwith 400 N follower load under two legstance condition. ROM indicates range ofmotion; SIJ, sacroiliac joint.

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Figure 5. Comparison of male and femaleintact left SIJ ROM at 10 Nm moment with400 N follower load under two leg stancecondition. ROM indicates range of motion;SIJ, sacroiliac joint.

BIOMECHANICS Sex Specific SIJ Biomechanics During Standing Upright � Joukar et al

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male model was 78% and 9% greater than the femalemodel, respectively.

Stresses Across SI JointThe maximum stress in the female model occurred duringthe left rotation, followed by flexion, right rotation, rightbending, left bending, and extension, Figure 6. In the malemodel, the greatest stress happened during the left rotation,followed by left bending, extension, flexion, right bending,and right rotation.

The maximum stresses at the female SIJ were higher by27% in flexion, 28% in right bending, 49% in left bending,45% in right rotation, and 20% in left rotation comparedwith those of the male model, Figure 6.

Sacrum had higher stresses compared with the ilium inboth models, Figure 6. Stresses at the female sacrum andilium were up to 49% and 29% greater than the male model.

Pelvis Ligaments StrainsFigures 7 and 8 show the results of the SIJ ligament strainsfor female and male models, respectively. The ASL strainswere the same during all motions. The LPSL experiencedgreatest tension during extension motion and had nostrain under the other motions. The SPSL was strainedmaximum during extension, but had comparable valuesunder the other loads. The ISL underwent the largest tensilestrains during all motions. The SSL and STL ligaments wereboth mostly strained during flexion, experienced similarvalues under other loads, and had no strain duringextension.

In the female model, ASL, LPSL, SPSL, and STL under-went larger strains compared with the corresponding male

Figure 6. Comparison of maximum stresseson the sacrum and ilium for intact femaleversus intact male at 10 Nm moment plus400 N follower load under two leg stancecondition.

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model ligaments, while SSL had similar values for bothsexes, and ISL showed greater strains in the male model.

Load Sharing across SI JointComputed load values, Tables 2 and 3 represent the greateraverage force magnitudes on the ilium and sacrum ofboth sides.

Female SIJs experienced higher loads across the jointscompared with the male SIJs under the similar loadingconditions. In both models, the shear loads were higherthan normal forces acting on the SIJ surfaces.

DISCUSSIONAlthough there are many studies which have quantified theROM, the literature on the biomechanical differencesbetween male and female SIJ is rare with only one studycomparing the ROM differences of SIJ between sexes.20

However, they did not provide load sharing and stress dataacross the SI joint. The current study showed that SIJ hadhigher mobility in females compared with males which is inagreement with the literature. In both male and femalemodels, the motion was minimum in lateral bending. Thegreatest difference of the SIJ motions between male andfemale models occurred during extension in which thefemale model showed significantly higher motion than themale model. The increased mobility in the female SIJ can beattributed to a lesser pronounced curvature of the SIJsurfaces, a larger gap (2 mm) at the SIJ, and a greater pubicangle (1118) compared with the male model which had1 mm gap at SIJ and pubic angle of 768.12,21

Anatomical study by Ebraheim and Biyani22 revealedthat the SIJ surface area is relatively greater in adult males

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TABLE 3. Load Sharing Across the Male SIJ Including Total, Shear, and Normal Loads for 10 NmMoment Plus 400 N Follower Load Under Two Leg Stance Condition

Motion Sex Total Load (N) Shear Load (N) Normal Load (N)

Flexion Male 192 190 16

Extension Male 161 142 31

RB Male 157 113 104

LB Male 223 221 18

RR Male 206 201 27

LR Male 155 153 12

LB indicates left bending; LR, left rotation; RB, right bending; RR, right rotation; SIJ, sacroiliac joint.

Figure 7. Average strains of female pelvisligaments for 10 Nm moment plus 400 Nfollower load under two leg stance condi-tion. ASL indicates anterior sacroiliac liga-ment; ISL, interosseous sacroiliac ligament;LPSL, long posterior sacroiliac ligament;SPSL, short posterior sacroiliac ligament;SSL, sacrospinous ligament; STL, sacrotu-berous ligament.

Figure 8. Average strains of male pelvisligaments for 10 Nm moment plus 400 Nfollower load under two leg stance condi-tion. ASL indicates anterior sacroiliac liga-ment; ISL, interosseous sacroiliac ligament;LPSL, long posterior sacroiliac ligament;SPSL, short posterior sacroiliac ligament;SSL, sacrospinous ligament; STL, sacrotu-berous ligament.

TABLE 2. Load Sharing Across the Female SIJ Including Total, Shear, and Normal Loads for 10 NmMoment Plus 400 N Follower Load Under Two Leg Stance Condition

Motion Sex Total Load (N) Shear Load (N) Normal Load (N)

Flexion Female 261 242 97

Extension Female 170 150 80

RB Female 308 281 126

LB Female 250 221 102

RR Female 254 205 142

LR Female 226 214 71

LB indicates left bending; LR, left rotation; RB, right bending; RR, right rotation.

BIOMECHANICS Sex Specific SIJ Biomechanics During Standing Upright � Joukar et al

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BIOMECHANICS Sex Specific SIJ Biomechanics During Standing Upright � Joukar et al

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than females. The smaller joint surface area in female SIJ canresult in higher local stresses across the joint. The currentstudy showed that the maximum stress values in the femalemodel were 49% higher than male model. The results ofcurrent study also showed that greater motion at the SIJresults in higher loads leading to higher stresses across thejoint under different motions, especially, on sacrum whichexperienced higher stresses compared with the ilium in bothsexes. This higher stress in females can result in higher risk ofSIJ pain and higher risk of sacral stress fracture.

Obtaining more quantitative information may be essen-tial to recognize SIJ dysfunction in both sexes due to the lackof quantitative relationship between the physiological spinemotion and the biomechanical factors such as ligamentstrain that may be associated with pain in the SIJ. In thecurrent study, the authors illustrated that depending on thespine motion, the ligament strains varied. The ASL, SPSL,STL, SSL, and ISL underwent tension to constrain the SIJduring flexion. LPSL is one of the posterior ligaments whichonly functions during extension. SSL and STL seem to haveno function in extension; however, SSL serves as a mainconstraint in other motions. Janssen et al23 have shown thatby sectioning sacrospinous and sacrotuberous ligaments, SIJstability decreased. The posterior sacroiliac ligaments con-tributed most to the SIJ mobility, while the anterior sacroil-iac ligaments had little influence24. Resisting the nutationand counternutation of the joint were done by ISL, STL,SSL, and LPSL25,26. The major role in stabilizing the SIJ wasdue to ISL, one of the strongest ligaments in the body.Interestingly, ASL, LPSL, SPSL, and STL underwent higherstrains in the female model and ISL stretched more in themale model. These high strains on certain ligaments in bothmodels can be explained by these anatomical differenceswhich females have smaller ASL, LPSL, and SPSL and maleshave smaller ISL compared with each other.7 Although inour models, ligaments had same properties in both models,but depending on the sex, the strain exerted on the ligamentswere different.

To our knowledge, this is the first study which investi-gated the difference between SIJ ROM of female and male aswell as stresses, load sharing, and ligaments strain across thejoint in different motions. The presented data can be used toaddress various critical questions regarding the anatomicaldifferences between male and female SIJ. For example,compared with men, who have a more ventral center ofgravity, in females the center of gravity commonly passes infront of or through the SIJ.27,28 This difference implies thatmen would have a greater lever arm than women, account-ing for the stronger SI joints in males.13 This characteristicmay explain why males have more restricted mobility.

One of the limitations of this study is the use of similarbone and ligaments material properties for the female andmale models due to the lack of experimental data.

In conclusion, this study found that the female SIJ hadrelatively higher ROM than male model at both sides of theSI joint. Also, the female SIJ experienced higher stressesacross the joint especially on the sacrum compared with

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males which implies that the females are at a higher risk ofstress fracture injury. The major role in stabilizing the SIJwas performed by ISL which is one of the strongest liga-ments in the body. The shear loads are higher across thefemale SIJ, compared with male SIJ. These differences maycontribute to higher incidence of LBP in females, includingduring pregnancy. We are presenting the details of modelformulations, both for a male and a female sample whichcan now be expanded and used to study sex differences inother postures and other conditions like pregnancy.

th

Key Points

oriz

Female SIJ had relatively higher range of motionthan male model at both sides of the SI joint.

Female SIJ experienced higher stresses across thejoint especially on the sacrum compared withmales which implies that the females are at ahigher risk of stress fracture injury.

Female model ligaments underwent larger strainscompared with the male model ligaments.

The shear loads are higher across the female SIJcompared with male SIJ.

ed

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