- Email: [email protected]
Ligamentous influence in pelvic load distribution
The Spine Journal
-
(2013)
-
Basic Science
Ligamentous influence in pelvic load distribution Niels Hammer, MDa,b,*, Hanno Steinke, PhDa, Uwe Lingslebe, MScb, Ingo Bechmann, MDa, Christoph Josten, MDb, Volker Slowik, PhDc, J€ org B€ ohme, MDb a Faculty of Medicine, Institute of Anatomy, University of Leipzig, Liebigstraße 13, 04103 Leipzig, Germany Department of Trauma and Reconstructive Surgery, Faculty of Medicine, University of Leipzig, Liebigstraße 13, 04103 Leipzig, Germany c Faculty of Civil Engineering & Architecture, Leipzig University of Applied Sciences (HTWK), Karl-Liebknecht-Straße 132, 04277 Leipzig, Germany b
Received 3 May 2012; revised 3 January 2013; accepted 20 March 2013
Abstract
BACKGROUND CONTEXT: The influence of the posterior pelvic ring ligaments on pelvic stability is poorly understood. Low back pain and sacroiliac joint (SIJ) pain are described being related to these ligaments. Computational approaches involving finite element (FE) modeling may aid to determine their influence. Previous FE models lacked in precise ligament geometries and material properties, which might have influence on the results. PURPOSE AND STUDY DESIGN: The aim of this study is to investigate ligamentous influence in pelvic stability by means of FE using precise ligament material properties and morphometries. METHODS: An FE model of the pelvis bones was created from computer tomography, including the pubic symphysis joint (PSJ) and the SIJ. Ligament data were used from 55 body donors: anterior (ASL), interosseous (ISL), and posterior (PSL) sacroiliac ligaments; iliolumbar (IL), inguinal (IN), pubic (PL), sacrospinous (SS), and sacrotuberous (ST) ligaments; and obturator membrane (OM). Stress-strain data were gained from iliotibial tract specimens. A vertical load of 600 N was applied. Pelvic motion related to altered ligament and cartilage stiffness was determined in a range of 50% to 200%. Ligament strain was investigated in the standing and sitting positions. RESULTS: Tensile and compressive stresses were found at the SIJ and the PSJ. The center of sacral motion was at the level of the second sacral vertebra. At the acetabula and the PSJ, higher ligament and cartilage stiffnesses decrease pelvic motion in the following order: SIJ cartilageOISLOSTþSSOILþASLþPSL. Similar effects were found for the sacrum (SIJ cartilage OISLOILþASLþPSL) but increased STþSS stiffnesses increased sacral motion. The influence of the IN, OM, and PL was less than 0.1%. Compared with standing, total ligament strain was reduced to 90%. Increased strains were found for the IL, ISL, and PSL. CONCLUSIONS: Posterior pelvic ring cartilage and ligaments significantly contribute to pelvic stability. Their effects are region- and stiffness dependent. While sitting, load concentrations occur at the IL, ISL, and PSL, which goes in coherence with the clinical findings of these ligaments serving as generators of low back pain. Ó 2013 Elsevier Inc. All rights reserved.
Keywords:
Biomechanics; Finite elements modeling; Iliolumbar ligament; Sacroiliac joint ligaments; Sacrospinous and sacrotuberous ligament
FDA device/drug status: Not applicable. Author disclosures: NH: Speaking/Teaching Arrangements: Teaching Anatomy (Salary as Research Assistant and Teacher, government paid); Fellowship Support: Yokochi and Kanehara Fund (Travel allowance and scholarship for cooperation with Japan, C USD). HS: Nothing to disclose. UL: Nothing to disclose. IB: Nothing to disclose. CJ: Nothing to disclose. VS: Speaking/Teaching Arrangements: Ingenium Education Austria (C); Research Support (Investigator Salary): Deutsche Forschungsgemeinsch aft (amount received for staff) (D); Research Support (Staff/Materials): 1529-9430/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.spinee.2013.03.050
Deutsche Forschungsgemeinsch aft (amount received for staff) (D). JB: Nothing to disclose. The disclosure key can be found on the Table of Contents and at www. TheSpineJournalOnline.com. NH and HS contributed equally to the manuscript. * Corresponding author. Faculty of Medicine, Institute of Anatomy, University of Leipzig, Liebigstraße 13, 04103 Leipzig, Germany. Tel.: (49) 341-97-22053; fax: (49) 341-97-22009. E-mail address: [email protected] (N. Hammer)
2
N. Hammer et al. / The Spine Journal
Introduction The influence of posterior pelvic ring ligaments on stability of the pelvis is discussed controversially. Low back pain and sacroiliac joint (SIJ) pain are commonly accepted to be related to pelvic ligament dysfunction [1,2]. The involvement of nociceptive neural elements located within the SIJ region underlines the involvement of ligaments as potential pain generators [3–5]. A significant influence of the sacroiliac ligaments (anterior [ASL], interosseous [ISL], and posterior [PSL] sacroiliac ligaments) was determined in the previous material testing [6–11]. Yet, little or no influence was found for the iliolumbar (IL), sacrospinous (SS), or sacrotuberous ligaments (ST) [6,10,11]. These findings are in contrast with anatomic studies [12–14], biomechanical studies [7,9,15], and with the widely accepted postulate that form and function cohere closely [16,17]. Assuming the biomechanical nonentity in regard to pelvic ligaments, surgical approaches were developed to transect the ligaments in nerve entrapment syndromes [18,19]. In pelvic trauma, pelvic ligaments are still underestimated in radiological and clinical diagnosis and in surgical treatment despite of the poor outcome after anatomic bone reconstruction [20–22]. This lack of consideration of pelvic ligaments may not only be caused by inadequate imaging techniques but also be related to insufficient, sparse information on the pelvic ligaments. Conclusively, questions concerning the function of the pelvic ligaments and their contribution to pelvic stability are unanswered until today. Computational approaches involving finite element (FE) modeling may aid to answer these still open questions. Yet, recent studies using FE lacked in precise geometries and material properties of the pelvic ligaments [23–28]. Additionally, existing results did not suffice to provide quantitative data, especially in concerns of the IL, SS, and ST [29]. New computational models are to be developed, focusing on ligaments to answer these still open
-
(2013)
-
questions about their influence in pelvic stability. This is the main issue of our study, including detailed morphometries of the posterior pelvic ring ligaments. The following hypotheses were addressed: A. An alteration of pelvic ligament or cartilage stiffness properties alters the extent of pelvic motion, proving their influence in stabilization. B. The SS and the ST ligaments significantly contribute to ligamentous effects of pelvic stabilization. C. Pelvic load distribution is different in the standing and sitting positions. Materials and methods Model construction: bones Bone geometry was based on computed tomography (CT) slices of a healthy male pelvis, using 1-mm slices of the pelvic ring [30,31]. Dicom data of both coxal bones and the sacrum of the body donor were imported to Ansys Workbench 12.0 (Ansys, Inc., Canonsburg, PA, USA; Fig. 1). Meshing was accomplished using the virtual topology feature and the patch-independent method for geometry-dependent mesh density [32,33]. The bones were meshed using tetrahedral (Solid187) elements, each consisting of 10 nodes. Material properties of cortical shell were assigned according to the previous literature [34] (Young modulus of elasticity E511,000 N/mm2, shear modulus m50.2). As a simplification, bone isotropy was presumed. Model construction: ligaments The following ligaments of the posterior pelvic ring were included (three-dimensional anatomic shapes): IL (cuboid), ASL (parallelepipeds), ISL (parallelepipeds), PSL (parallelepipeds), SS (frustum), and ST (bifrustum).
Fig. 1. Import of geometries and modeling of the sacroiliac joint (SIJ) Dicom data of both coxal bones (C) and the sacrum (S) were imported to Ansys Workbench 12.0 (Ansys, Inc., Canonsburg, PA, USA). (Left) The anterior view of the meshed bones and (Right) the lateral view at the sacral part of the left SIJ. P, promontory; a, anterior; cd, caudal; cr, cranial; l, left; p, posterior; r, right; scale bar550 mm (left), 25 mm (right).
N. Hammer et al. / The Spine Journal
Ligament morphometry was based on gender-dependent data gained from the anatomic dissection of 55 body donors and CT, 7-T magnetic resonance imaging, and corresponding thin slice plastination of another three body donors [35–37]. Ligament lengths, widths, heights, angles, origin and insertion areas, and fiber orientations were included. Additionally, the obturator membrane and the inguinal and the pubic ligaments were included [38,39]. Meshing was accomplished, using link elements (Fig. 1, Table 1; Link180, large displacement, tension only). Two remote points were defined for each link element, representing one of the main fiber directions within the ligament with the given morphometry. Because of lacking data on pelvic ligament tensile properties, we used the previously published data of the iliotibial tract [40] (E5397 N/mm2). Model construction: joints The SIJ was modeled as a partitioned volume. The ventral cartilaginous part consisted of the auricular surface. The dorsal ligamentous part consisted of the ISL with the given geometry [29,37] (Fig. 2). The pubic symphysis joint (PSJ) was modeled using the published data [38,39]. Material properties of cartilage were assigned for the ventral part of the SIJ and for PSJ according to Guess et al. [41] (E5150 N/mm2, m50.2). Boundary conditions A pelvic inclination of 60 was presumed to simulate gravity effects on the pelvis in the standing position [42,43]. For horizontal loads of the pelvis, a femoral caputcollum-diaphyseal angle of 121 was assumed [44]. The sacrum was defined as a fixed bearing. Because of the missing fifth lumbar vertebra, the origin of the IL was set as a boundary condition with fixed coordinates. The total pelvic load was chosen to be 600 N, equally distributed to both acetabula. Table 1 Ligament load distribution in the standing and the sitting positions Load distribution (%) Ligament
Number of elements
Standing
Sitting
IN PL OM IL ASL ISL PSL SS ST
1 2 1 2 9 5 9 3 3
0.00 0.00 0.12 14.72 12.95 3.57 1.09 39.42 28.12
0.00 0.00 0.12 15.02 12.85 3.75 1.14 39.22 27.90
ASL, anterior sacroiliac ligament; IN, inguinal; PL, pubic; SS, sacrospinous; ST, sacrotuberous ligament; OM, obturator membrane; IL, iliolumbar; ISL, interosseous sacroiliac ligament; and PSL, posterior sacroiliac ligament. Note: The number of elements used for the finite element simulation and relative ligament strain distribution (%) is given for the pelvic ligaments in the standing and the sitting positions. While total pelvic load decreased, strain concentrations were found for the IL, ISL, and PSL.
-
(2013)
-
3
Outcome variables Ten computational substeps were used in the investigation of each outcome variable. The use of each substep served as a verification of material deformation, checking the accuracy of the stiffness matrix and the osteoligamentous model for plausibility: 1. Pelvic motion related to load application was examined. 2. Load distribution of the PSJ and of the SIJ was evaluated graphically by means of a vector presentation. 3. The influence of pelvic ligament and SIJ cartilage material properties to pelvic motion was analyzed. Pelvic ligaments were grouped as follows: inguinal and pubic ligaments, ISL, ILþASLþPSL, and SSþST. Three points were examined at the bony pelvis, averaging the values of both sides if applicable: PSJ (cranial tip), sacral base, and point of load application at the acetabulum. Ligament and cartilage material properties were altered in a range of 50% to 200% (75 N/mm2#Ecartilage#300 N/mm2; 198 N/mm2#Eligament#794 N/mm2}. 4. Relative ligament strain in the sitting and the standing positions was finally computed. Pelvic inclination and femoral tilt were adapted to both load scenarios [45]. The outcome variables of (1) to (3) were calculated in Ansys workbench. The load scenarios were computed in Ansys classic, using Ansys Parametric Design Language. Model validation Load-deformation data were recorded from seven male unembalmed hemipelves (Table 2, mean age 81.576 10.75 years) [29,46]. While alive, the body donors gave informed consent to the donation of their bodies for scientific and educational purposes. The hemipelves were attached to a steel plate with three 8-mm steel screws: one was fixed to the spine at fifth lumbar vertebra and two were fixed to the fourth and fifth sacral vertebrae. An LFEM 600/100/10 material testing machine (WalterþBai, L€ohningen, Switzerland) was used, applying a maximum load of 260 N to the acetabulum by means of a hip joint prosthesis (ABG II H€uftsystem; Stryker GmbH & Co. KG, Duisburg, Germany). Pelvic motion was recorded at the cranial tip of the PSJ and at the acetabulum, using type W10TK displacement transducers, MGL Plus amplifiers, and the Catman software (Hottinger Baldwin Messtechnik GmbH, Darmstadt, Germany). The data of the materials testing were compared with the results of the FE simulation at the following points: ilium (posterior superior iliac spine), acetabulum, and PSJ. Results The pelvic model consisting of the coxal bones, the sacrum, and adjacent ligaments was constructed, using
4
N. Hammer et al. / The Spine Journal
-
(2013)
-
Fig. 2. Modeling of pelvic ligaments. The pelvic ligaments were modeled as link elements, based on precise measurements. The ventral (A), lateral (B), dorsal (C), and cranial (D) views are shown. ASL, anterior sacroiliac ligament; IL, iliolumbar; IN, inguinal; OM, obturator membrane; PL, pubic ligament; PSL, posterior sacroiliac ligament; SS, sacrospinous ligament; ST, sacrotuberous ligament; a, anterior; cd, caudal; cr, cranial; l, left; p, posterior; r, right; scale bar550 mm (A–C), 70 mm (D).
approximately 155,000 elements. A total of 66 link elements were used for all ligaments and the OM (Figs. 1 and 2). Pelvic motion related to load application Applying a vertical load to both acetabula, total PSJ motion was 0.47 mm (Fig. 3). The sacral promontory rotated Table 2 Body donors
caudally and ventrally and the apex of the sacrum rotated cranially and dorsally. Sacral rotation was limited by the SS and ST. The center of rotation is located at the level of second sacral vertebra, depicted as the region of least motion. Both iliac crests were more distant from the sacrum in the loaded condition, compared with the unloaded condition. Load distribution at the PSJ and SIJ
Specimen
Age (y)
Pelvis side
1 2 3 4 5 6 7 Mean6SD
60 75 83 87 88 88 90 81.57
Left Left Left Left Left Right Left 10.75
SD, standard deviation. Note: The age of the body donors is given along with the hemipelvis side used for biomechanical validation.
At the PSJ, tensile stress was found at the cranial and ventral aspect of the pubic arch (Fig. 4, Left, red vectors). More dorsally and caudally at the PSJ, compressive stress was observed (blue). The intermediate region is characterized by both compressive and tensile stresses with different vectors, resulting in bending stress (green vectors, Fig. 4, Left and Middle). Fig. 4, Right, shows the load distribution at the SIJ. Compressive stress was found ventrally in the region of the auricular surface covered with cartilage. Dorsally, tensile stress was observed in the ligament region. Tensile stress was concentrated in the
N. Hammer et al. / The Spine Journal
-
(2013)
-
5
Fig. 3. Load-displacement results of the osteoligamentous finite element model, depicted in red (left). Maximum displacements were measured at the pubic symphysis with 0.47 mm, depicted in red. The promontory (P) rotated caudally and ventrally. The center sacral motion is at the level of the second sacral vertebra, depicted in blue (right). C, coxal bone; S, sacrum; a, anterior; cd, caudal; cr, cranial; l, left; p, posterior; r, right; scale bar550 mm.
dorsal and cranial SIJ compartment with the ISL and PSL. At level of the second sacral vertebra (center of rotation), least compressive and tensile stresses were observed. The influence of ligament and cartilage material properties in pelvic motion An increase of SIJ cartilage and ligament material stiffnesses decreased pelvic motion at all the observed points
with one exception: higher SSþST stiffnesses increased sacral motion. The results are given in Fig. 5. The following order was observed regarding the magnitude of motion, caused by altered ligament and cartilage properties: at the PSJ and acetabulum, alteration of SIJ cartilage stiffnesses had most influence, followed by ISL, SSþST, and ILþASLþPSL, and at the sacral base, SSþST’ stiffness had most influence, followed by SIJ cartilage, ISL, and ILþASLþPSL. Alteration of inguinal and pubic ligaments’
Fig. 4. Load distribution at the pubic symphysis joint (PSJ) and sacroiliac joint (SIJ). The SIJ (Left, lateral view) is characterized by compression in the ventral (cartilaginous) region and by tension in the dorsal ligamentous region. Least stress-strain was observed at the level of the second sacral vertebra, and strain concentration was located in the cranial and dorsal regions of the iliolumbar, the interosseous, and posterior sacroiliac ligaments, indicated by red arrows. At the PSJ (Middle, ventral view; Right, lateral view), compression was observed dorsally and caudally. The intermediate and cranial regions are characterized by both compression and tension with different vectors, resulting in bending stress. a, anterior; cd, caudal; cr, cranial; l, left; p, posterior; r, right; blue vectors: compressive force; red vectors: strain; green vectors: torsional/bending stress; scale bar515 mm (Left), 4 mm (Middle and Right).
6
N. Hammer et al. / The Spine Journal
-
(2013)
-
Model validation In the comparison of the load-deformation data of the hemipelves with the FE model at the given points, displacement directions matched (Fig. 6). Pelvic deformation of the body donors was one magnitude larger.
Discussion Biomechanical and clinical observations
Fig. 5. Influence of cartilage and ligament properties on the extent of pelvic motion. An increase of SIJ cartilage and ligament material stiffnesses decreased pelvic motion at all the observed points (Top, Middle, and Bottom) with one exception: higher STþSS stiffnesses increased sacral motion (Top). SS, sacrospinous; ST, sacrotuberous ligament; PL, pubic ligament; OM, obturator membrane; IL, iliolumbar; ASL, anterior sacroiliac ligament; PSL, posterior sacroiliac ligament; IN, inguinal; ISL, interosseous sacroiliac ligament; SIJ, sacroiliac joint.
stiffnesses resulted in least alteration of motion at all the observed points (O0.1%). Relative ligament strain in the sitting and the standing positions The resulting vectors applied to both acetabula were x5180.26 N, y5150.00 N, and z5259.81 N for the standing position (pelvic inclination560 ) and x5180.23 N, y5251.60 N, and z5163.39 N for the sitting position (pelvic inclination533 ). In contrast, ligament strain increased within the IL, ISL, and PSL (Table 1).
In accordance to the previous literature [7,15,47], the stabilizing function of the ASL, ISL, and PSL was confirmed by recent biomechanical tests [10,11,46,48] and with our virtual setup. Scolumb and Terry [15], Miller et al. [48], and Rothk€otter and Berner [8] recorded the load-displacement behavior and the failure characteristics of the SIJ in biomechanical testing of a large number of specimens. Yet, no distinction of the ISL and PSL could be made with regard to their individual influence in pelvic stability. Little influence was found for the IL, SS, and ST as stabilizers [6,10,11], which mismatched with other findings [49–52]. Based on this ‘‘lack of function,’’ surgical transection of the SS and ST was developed for the pudendal nerve entrapment syndrome [18,19]. The major limitation of the studies of Philippeau et al. [18] and Vrahas et al. [10] was that they exclusively performed material testing with axial loads of the SIJ, neglecting the multiaxial nature of the SIJ and its nutation movement [12]. In a similar manner, Vukicevic et al. [11] applied double sandwich interferometry in a setup that prevented the pelvis from tilting. Doing so, the SS and ST possibly remained unloaded [10,11,18]. Conza et al. [6] applied one dimensional laser vibrometry in a range of 10 to 340 Hz in one specimen and determined no influence of the IL, SS, and ST in pelvic stability. Their conclusions can be rebutted by PoolGoudzwaard et al. [51] in mechanical tests of 12 donors and by our findings. Also, Neugebauer et al. [53] found out that the pelvis is best characterized at frequencies between 500 and 2,000 Hz using three-dimensional laser vibrometries in a much larger specimen number than Conza et al. [6]. Proving hypotheses (A) and (B), our study confirms significant influence of all posterior pelvic ring ligaments on stabilization—including the IL, SS, and ST. Alteration of pelvic motion was observed, related to altered ligament and cartilage properties. At the acetabula and the PSJ, SIJ cartilage properties mostly reduce motion, followed by the SS and ST, the ISL, and the group of IL, ASL, and PSL properties. At the sacrum, SIJ cartilage reduces pelvic motion to the largest extent, followed by the ISL and the group of IL, ASL, and PSL. An opposite effect was determined for the SS and ST: increased stiffnesses caused increased sacral motion. This is reasonable, when looking at the boundary conditions that defined the top of the
N. Hammer et al. / The Spine Journal
-
(2013)
-
7
force transmission with subsequent axial rotation and translation. At the SIJ, the lever ratio of the SS and ST is more effective, compared with the ISL with a larger crosssectional area [37]. Because of these effects, the influence of the SS and ST is weakened at the acetabula and the PSJ. Here, the lever arms of the SIJ cartilage and ISL are more effective. The inguinal and pubic ligaments had least influence on alteration of pelvic motion, which might be the result of cumulative effects to neutralize stresses at the PSJ [38,39]. In our graphical evaluation (Fig. 3), the center of axial rotation was determined within the ISL at level of second sacral vertebra, which complies with previous studies [54] and the previous description of the ISL as Achsenband [55,56]. Compressive, tensile, and shear forces were found for the PSJ and SIJ, which confirms biomechanical [38,39] and histologic findings [12,57,58]. Alterations in cartilage material properties, for example related to arthritis or arthrosis elsewhere [59], significantly affect pelvic motion. In accordance with hypothesis (C), alterations of load distributions were found for the sitting position, compared with standing. Local strain concentrations were determined at the IL, ISL, and PSL. These findings confirm that nerve endings located within the SIJ and IL ligaments [9,60–62] may serve as generators of low back pain during ligament strain [51,63]. This effect can be increased in the sitting position or by so-called slouching movements [64]. Comparison with other FE simulations
Fig. 6. Comparison of load-deformation data of the hemipelves with the finite element (FE) model. In the validation with the body donors, displacement directions matched. The ilium (Top, posterior superior iliac spine), acetabulum (Middle), and pubic symphysis joint (Bottom) were observed. Deformations of the body donors (circles) were one magnitude larger, compared with the FE simulation (triangles).
sacrum as a fixed support. The influence can be explained by the geometry and the cross-sectional areas of the aforementioned ligaments [14,15,40,47]. The SS and ST directly connect the ischium to the distal sacrum, causing direct
Few FE studies on posterior pelvic ring ligaments are available in literature. These studies were based on hemipelves [23,24,26], fixed SIJ [25], or on limited ligament data [24,27–29,65]. Investigators of posterior pelvic ring morphometries faced two problems: first, the ligaments situated inside the SIJ could not be measured sufficiently and were, therefore, estimated [14,66,67] and second, measurements of a small number of specimens may neither represent the standard case nor allow using gender-dependent data [68–70]. Third, previous measurements were optimized for anthropological purposes, not for virtual biomechanics. Geometries of ligaments influence the results of biomechanical and virtual simulations [71]. We previously determined anatomic data of the posterior pelvic ring ligament geometries for the given FE model [35–37]. Anatomic preparations and frozen sections were accomplished in pelves of 55 body donors along with correlating CT, 7-T magnetic resonance imaging, and thin slice plastination in another 3 donors. Using these techniques, an in situ visualization and description of the ligaments were possible. Another issue to be addressed is the lack of stiffness properties of pelvic ring ligaments. Existing literature only provides load-displacement data of the entire pelvic ring [7,8] or of the isolated SIJ [48]. Because of the complexity of the SIJ ligaments and their anatomic location being surrounded by the sacrum and the coxal bones, their strain data
8
N. Hammer et al. / The Spine Journal
can presently only be estimated. Reliable stress-strain properties of the IL, SS, and ST are presently not available. Some FE simulations included numerically estimated data [25,28,65] or published data of the human knee ligaments [27]. Because these material properties may not be true for the pelvic ligaments, we decided to use iliotibial tract material properties [40]. The tract is none of the ligaments considered in our FE model, but its material data may be more reasonable than knee data because of its topographical proximity and influence on pelvic mechanics. Additionally, its parallel fibers allowed precise measurements. The main results of previous FE studies can be confirmed and extended with our present investigation. The IL, ASL, ISL, and PSL are involved in horizontal load transfer at the acetabulum and ilium [29]. The SS and ST provide vertical load transfer with subsequent translation of the sacrum [29]. These results were now quantified. Eichenseer et al. [27] found that decreasing ligament stiffnesses increase SIJ stress and angular motion with maximum strains at the ISL. This is can be confirmed for all ligaments except for the SS and ST. The latter ligaments increase sacral motion at increasing stiffnesses. Ligament-related differences in stress-strain fields, as observed by Phillips et al. [25], are, therefore, reasonable because of different ligament effects at different locations of the pelvis. Validation and limitations Finite element modeling is a simplification of the functional anatomy of biological tissues. Only structures that have actually been included into the models can be observed with regard to their function. In our present model, no muscles have been integrated. The erector spinae, the quadratus lumborum [72,73], abdominal wall muscles [4,74,75], the gluteus maximus [73,76,77], and further muscles [75,78] were found to exert influence on pelvic ring and the SIJ. Despite this simplification, FE modeling may aid to determine ligament and joint mechanics if standard material testing will not give satisfactory results. This is especially true for the ISL, SS, and ST. Rigid isotropic properties were attributed to the bones, which is a simplification with effects on our validation data with the body donors. Although the direction of motion is equal for all points, in situ motion with body donors is one magnitude higher than computed in our model. Also, hemipelves of body donors are compared with a complete pelvis investigated that might have an effect on the validation. Yet, the maximum pelvic displacement in our model was 0.47 mm at the PSJ (load 600 N), which is comparable with the published data ([48]: 0.28 mm at 294 N, [8]: 0.45 mm at 600 N). The origin at the IL was defined as a fixed boundary condition because of missing data of the fifth lumbar vertebra. Motion of lumbosacral transition was excluded. Being aware of these limitations of the osseous components, ligamentous influence on the pelvic ring could be observed successfully with our model, proving the three hypotheses. Although the
-
(2013)
-
iliotibial tract overspans the pelvis and the hip joint, it might not necessarily reflect the mechanical characteristics of the posterior pelvic ring ligaments but seems to be more justifiable than knee ligaments [27]. Stress-strain data gained from the posterior pelvic ring ligaments will have to be integrated into future models. Models that integrate these data along with muscle loads and anisotropic data of cortical and cancellous bone may be the next step. Further optimization of structural geometry may aid to reduce the error probability and shorten computational time.
Conclusions and outlook This is the first study to determine the influence of posterior pelvic ligaments in pelvic motion, based on detailed morphometries. Posterior pelvic ring cartilage and ligaments significantly contribute to pelvic stability. Ligamentous effects on the bony pelvis are region- and stiffness dependent. The SS and ST significantly contribute to ligament stability of the pelvis. Total ligament strain is larger in the standing position, compared with the sitting position. In the sitting position, load concentrations occur at the IL, ISL, and PSL, which goes in coherence with the clinical findings of these ligaments serving as generators of low back pain [9,64,79]. Further clinical questioning may be answered in regard to low back pain and to surgical treatment of ligaments in pelvic fractures, using osteoligamentous FE models. References [1] Cohen SP. Sacroiliac joint pain: a comprehensive review of anatomy, diagnosis, and treatment. Anesth Analg 2005;101:1440–53. [2] Fortin JD, Vilensky JA, Merkel GJ. Can the sacroiliac joint cause sciatica? Pain Physician 2003;6:269–71. [3] Damen L, Spoor CW, Snijders CJ, Stam HJ. Does a pelvic belt influence sacroiliac joint laxity? Clin Biomech (Bristol, Avon) 2002; 17:495–8. [4] Mens JMA, Damen L, Snijders CJ, Stam HJ. The mechanical effect of a pelvic belt in patients with pregnancy-related pelvic pain. Clin Biomech (Bristol, Avon) 2006;21:122–7. [5] Pel JJM, Spoor CW, Goossens RHM, Pool-Goudzwaard AL. Biomechanical model study of pelvic belt influence on muscle and ligament forces. J Biomech 2008;41:1878–84. [6] Conza NE, Rixen DJ, Plomp S. Vibration testing of a fresh-frozen human pelvis: the role of the pelvic ligaments. J Biomech 2007; 40:1599–605. [7] Fessler J. Die Festigkeit der menschlichen Gelenke mit besonderer Ber€ucksichtigung des Bandapparates. Habilitationsschrift. M€unchen, Germany, 1894. [8] Rothk€otter HJ, Berner W. Failure load and displacement of the human sacroiliac joint under in vitro loading. Arch Orthop Trauma Surg 1988;107:283–7. [9] Varga E, Dudas B, Tile M. Putative proprioceptive function of the pelvic ligaments: biomechanical and histological studies. Injury 2008;39:858–64. [10] Vrahas M, Hern TC, Diangelo D, et al. Ligamentous contributions to pelvic stability. Orthopedics 1995;18:271–4. [11] Vukicevic S, Marusic A, Stavljenic A, et al. Holographic analysis of the human pelvis. Spine 1991;16:209–14.
N. Hammer et al. / The Spine Journal [12] Kapandji IA. Funktionelle Anatomie der Gelenke: Schematisierte und kommentierte Zeichnungen zur menschlichen Biomechanik: einb€andige Ausgabe—obere Extremit€at, untere Extremit€at, Rumpf und Wirbels€aule. 5th ed. Stuttgart, Germany: Thieme, 2009. [13] Tittel K. Beschreibende und funktionelle Anatomie des Menschen. 14th ed. M€ unchen, Germany: Urban & Fischer, 2003. [14] Weisl H. The ligaments of the sacro-iliac joint examined with particular reference to their function. Acta Anat (Basel) 1954;20: 201–13. [15] Scolumb L, Terry R. Influence of the sacrotuberous and sacrospinous ligaments in limited movements of the sacroiliac joint. J Am Med Assoc 1926;87:307–9. [16] Pauwels F. Eine neue Theorie €uber den Einfluss mechanischer Reize auf die Differenzierung der St€utzgewebe. Zehnter Beitrag zur funktionellen Anatomie und kausalen Morphologie des St€utzapparates. Z Anat Entwicklungsgesch 1960;121. [17] Russell ES. Form and function: a contribution to the history of animal morphology. London, UK: Murray, 1916. [18] Philippeau J, Hamel O, Pecot J, Robert R. R^ole biomecanique des ligaments sacroepineux et sacrotuberal sur la stabilite de l’articulation sacro-iliaque. Anatomie et etude experimentale originale. Morphologie 2008;92:16–30. [19] Robert R, Prat-Pradal D, Labat JJ, et al. Anatomic basis of chronic perineal pain: role of the pudendal nerve. Surg Radiol Anat 1998; 20:93–8. [20] Burkhardt M, Culemann U, Seekamp A, Pohlemann T. Operative Versorgungsstrategien beim Polytrauma mit Beckenfraktur. Eine Literatur€ ubersicht. Unfallchirurg 2005;108:812. 814–820. [21] G€ansslen A, Pohlemann T, Paul C, et al. Epidemiology of pelvic ring injuries. Injury 1996;27(1 Suppl):SA13–20. [22] Pohlemann T, Tscherne H, Baumg€artel F, et al. Beckenverletzungen: € €uber die Epidemiologie, Therapie und Langzeitverlauf. Ubersicht multizentrische Studie der Arbeitsgruppe Becken. Unfallchirurg 1996;99:160–7. [23] Dalstra M, Huiskes R, van Erning L. Development and validation of a three-dimensional finite element model of the pelvic bone. J Biomech Eng 1995;117:272–8. [24] Murakami H, Kawahara N, Tomita K, et al. Biomechanical evaluation of reconstructed lumbosacral spine after total sacrectomy. J Orthop Sci 2002;7:658–64. [25] Phillips ATM, Pankaj P, Howie CR, et al. Finite element modelling of the pelvis: inclusion of muscular and ligamentous boundary conditions. Med Eng Phys 2007;29:739–48. [26] Anderson AE, Peters CL, Tuttle BD, Weiss JA. Subject-specific finite element model of the pelvis: development, validation and sensitivity studies. J Biomech Eng 2005;127:364–73. [27] Eichenseer PH, Sybert DR, Cotton JR. A finite element analysis of sacroiliac joint ligaments in response to different loading conditions. Spine 2011;36:E1446–52. [28] Garcıa JM, Doblare M, Seral B, et al. Three-dimensional finite element analysis of several internal and external pelvis fixations. J Biomech Eng 2000;122:516–22. [29] B€ ohme J, Steinke H, H€ulse R, et al. Komplexe ligament€are Instabilit€aten nach "open book"-Verletzungen des Beckenrings— Finite-Elemente-Computersimulation und Bruchversuch. Z Orthop Unfall 2011;149:83–9. [30] Shim VB, Pitto RP, Streicher RM, et al. The use of sparse CT datasets for auto-generating accurate FE models of the femur and pelvis. J Biomech 2007;40:26–35. [31] Shim VB, Pitto RP, Streicher RM, et al. Development and validation of patient-specific finite element models of the hemipelvis generated from a sparse CT data set. J Biomech Eng 2008;130: 51010. [32] Lawrence KL. ANSYS Workbench Tutorial: structural & thermal analysis using the ANSYS workbench release 11.0 environment. Mission, KS: Schroff Development Corp., 2007.
-
(2013)
-
9
[33] Lee H. Finite element simulations with ANSYS workbench 12: theory, applications, case studies. Mission, KS: Schroff Development Corp., 2010. [34] Wirtz DC, Schiffers N, Pandorf T, et al. Critical evaluation of known bone material properties to realize anisotropic FE-simulation of the proximal femur. J Biomech 2000;33:1325–30. [35] Hammer N, Steinke H, B€ohme J, et al. Description of the iliolumbar ligament for computer-assisted reconstruction. Ann Anat 2010;192: 162–7. [36] Hammer N, Steinke H, Slowik V, et al. The sacrotuberous and the sacrospinous ligament—a virtual reconstruction. Ann Anat 2009; 191:417–25. [37] Steinke H, Hammer N, Slowik V, et al. Novel insights into the sacroiliac joint ligaments. Spine 2010;35:257–63. [38] Li Z, Alonso JE, Kim J, et al. Three-dimensional finite element models of the human pubic symphysis with viscohyperelastic soft tissues. Ann Biomed Eng 2006;34:1452–62. [39] Li Z, Kim J, Davidson JS, et al. Biomechanical response of the pubic symphysis in lateral pelvic impacts: a finite element study. J Biomech 2007;40:2758–66. [40] Steinke H, Lingslebe U, B€ohme J, et al. Deformation behavior of the iliotibial tract under different states of fixation. Med Eng Phys 2012; 34:1221–7. [41] Guess TM, Thiagarajan G, Kia M, Mishra M. A subject specific multibody model of the knee with menisci. Med Eng Phys 2010; 32:505–15. [42] Boulay C, Tardieu C, Hecquet J, et al. Sagittal alignment of spine and pelvis regulated by pelvic incidence: standard values and prediction of lordosis. Eur Spine J 2006;15:415–22. [43] Le Demany P. L’angle sacro-pelvien, ses variations professionnelles. J Anat Physiol Norm Pathol Homm Anim 1909;45:276–87. [44] Alverdes K. Grundlagen der Anatomie. 3rd ed. Leipzig, Germany: VEB Georg Thieme, 1956. [45] H€ulse R, Hammer N, Steinke H, et al. Finite Elemente Modell des Beckens zur Simulation komplexer ligament€arer Instabilit€atsszenarien. In: Meinzer HP, Deserno TM, Handels H, Tolxdorff T, eds. Bildverarbeitung f€ur die Medizin 2009: Algorithmen, Systeme, Anwendungen: Proceedings des Workshops vom 22. bis 25. M€arz 2009 in Heidelberg. Berlin, Germany: Springer, 2009: 434–8. [46] Krause M. Experimentelle Untersuchung zum Verformungsverhalten des menschlichen Beckenrings. Leipzig, Germany: Diplomarbeit, 2007. [47] Weber W, Weber E. Die Mechanik der menschlichen Gehwerkzeuge: Eine anatomisch-physiologische Untersuchung. G€ottingen, Germany: Dieterichsche Buchhandlung, 1836. [48] Miller JA, Schultz AB, Andersson GB. Load-displacement behavior of sacroiliac joints. J Orthop Res 1987;5:92–101. [49] Basadonna PT, Gasparini D, Rucco V. Iliolumbar ligament insertions. In vivo anatomic study. Spine 1996;21:2313–6. [50] Hartford JM, McCullen GM, Harris R, Brown CC. The iliolumbar ligament: three-dimensional volume imaging and computer reformatting by magnetic resonance: a technical note. Spine 2000;25: 1098–103. [51] Pool-Goudzwaard A, van Hoek Dijke G, Mulder P, et al. The iliolumbar ligament: its influence on stability of the sacroiliac joint. Clin Biomech (Bristol, Avon) 2003;18:99–105. [52] Sims JA, Moorman SJ. The role of the iliolumbar ligament in low back pain. Med Hypotheses 1996;46:511–5. [53] Neugebauer R, Werner M, Voigt C, et al. Experimental modal analysis on fresh-frozen human hemipelvic bones employing a 3D laser vibrometer for the purpose of modal parameter identification. J Biomech 2011;44:1610–3. [54] Puhakka KB, Melsen F, Jurik AG, et al. MR imaging of the normal sacroiliac joint with correlation to histology. Skeletal Radiol 2004; 33:15–28.
10
N. Hammer et al. / The Spine Journal
[55] Farabeuf L. Sur l’anatomie et la physiologie des articulations sacroiliaques avant et apres la symphyseotomie. Gynecol Obstet (Paris) 1894;41:407–20. [56] Klein G. Zur Mechanik des Ileosacralgelenkes. Ann Anat 1891;6: 74–118. [57] Bennemann R. Untersuchungen am Iliosakralgelenk des Menschen. Verh Anat Ges 1979;73:187–90. [58] Tillmann B. Funktionelle Anpassung an Gelenken mit unterschiedlichem Belastungsmodus. Langenbecks Arch Chir Suppl II Verh Dtsch Ges Chir 1989;459–64. [59] G€ orke U, G€ unther H, Nagel T, Wimmer MA. A large strain material model for soft tissues with functionally graded properties. J Biomech Eng 2010;132:74502. [60] Bogduk N, Macintosh JE. The applied anatomy of the thoracolumbar fascia. Spine 1984;9:164–70. [61] Kellgren J. On the distribution of pain arising from deep somatic structures with charts of segmental pain areas. Clin Sci 1939;4: 35–46. [62] Szadek KM, Hoogland PVJM, Zuurmond WW, et al. Possible nociceptive structures in the sacroiliac joint cartilage: an immunohistochemical study. Clin Anat 2010;23:192–8. [63] Snijders CJ, Hermans PFG, Niesing R, et al. The influence of slouching and lumbar support on iliolumbar ligaments, intervertebral discs and sacroiliac joints. Clin Biomech (Bristol, Avon) 2004;19:323–9. [64] Snijders CJ, Hermans PFG, Niesing R, et al. Effects of slouching and muscle contraction on the strain of the iliolumbar ligament. Man Ther 2008;13:325–33. [65] Zheng N, Watson LG, Yong-Hing K. Biomechanical modelling of the human sacroiliac joint. Med Biol Eng Comput 1997;35:77–82. [66] Attias N, Arzani S, Duncan G, et al. Sectional imaging anatomy: pelvic ring ligaments. J Comput Assist Tomogr 2001;25:975–9. [67] Rosatelli AL, Agur AM, Chhaya S. Anatomy of the interosseous region of the sacroiliac joint. J Orthop Sports Phys Ther 2006;36: 200–8. [68] Gerlach UJ, Lierse W. Functional construction of the sacroiliac ligamentous. Acta Anat (Basel) 1992;144:97–102.
-
(2013)
-
[69] Remy M, Bouillet P, Bertin P, et al. Evaluation of magnetic resonance imaging for the detection of sacroiliitis in patients with early seronegative spondylarthropathy. Rev Rhum Engl Ed 1996;63: 577–83. [70] Seizeur R, Forlodou P, Person H, et al. The morphometric study of the sacrospinal and sacrotuberal ligaments correlated with the morphometry of the pelvis. Surg Radiol Anat 2005;27:517–23. [71] Lanovaz JL, Ellis RE. A cadaverically evaluated dynamic FEM model of closed-chain TKR mechanics. J Biomech Eng 2009;131:51002. [72] Park K, Kim S, Oh D. Effects of the pelvic compression belt on gluteus medius, quadratus lumborum, and lumbar multifidus activities during side-lying hip abduction. J Electromyogr Kinesiol 2010;20: 1141–5. [73] Takasaki H, Iizawa T, Hall T, et al. The influence of increasing sacroiliac joint force closure on the hip and lumbar spine extensor muscle firing pattern. Man Ther 2009;14:484–9. [74] Beales DJ, O’Sullivan PB, Briffa NK. The effects of manual pelvic compression on trunk motor control during an active straight leg raise in chronic pelvic girdle pain subjects. Man Ther 2010;15:190–9. [75] Hu H, Meijer OG, van Die€en JH, et al. Muscle activity during the active straight leg raise (ASLR), and the effects of a pelvic belt on the ASLR and on treadmill walking. J Biomech 2010;43:532–9. [76] Arumugam A, Milosavljevic S, Woodley S, Sole G. Effects of external pelvic compression on form closure, force closure, and neuromotor control of the lumbopelvic spine—a systematic review. Man Ther 2012;17:275–84. [77] Massoud Arab A, Reza Nourbakhsh M, Mohammadifar A. The relationship between hamstring length and gluteal muscle strength in individuals with sacroiliac joint dysfunction. J Man Manip Ther 2011;19:5–10. [78] Jung H, Jeon H, Oh D, Kwon O. Effect of the pelvic compression belt on the hip extensor activation patterns of sacroiliac joint pain patients during one-leg standing: a pilot study. 2012 Oct 27. [Epub ahead of print]. http://dx.doi.org/10.1016/j.math.2012.09.003. [79] Vleeming A, Stoeckart R, Volkers AC, Snijders CJ. Relation between form and function in the sacroiliac joint. Part I: clinical anatomical aspects. Spine 1990;15:130–2.
-
(2013)
-
Basic Science
Ligamentous influence in pelvic load distribution Niels Hammer, MDa,b,*, Hanno Steinke, PhDa, Uwe Lingslebe, MScb, Ingo Bechmann, MDa, Christoph Josten, MDb, Volker Slowik, PhDc, J€ org B€ ohme, MDb a Faculty of Medicine, Institute of Anatomy, University of Leipzig, Liebigstraße 13, 04103 Leipzig, Germany Department of Trauma and Reconstructive Surgery, Faculty of Medicine, University of Leipzig, Liebigstraße 13, 04103 Leipzig, Germany c Faculty of Civil Engineering & Architecture, Leipzig University of Applied Sciences (HTWK), Karl-Liebknecht-Straße 132, 04277 Leipzig, Germany b
Received 3 May 2012; revised 3 January 2013; accepted 20 March 2013
Abstract
BACKGROUND CONTEXT: The influence of the posterior pelvic ring ligaments on pelvic stability is poorly understood. Low back pain and sacroiliac joint (SIJ) pain are described being related to these ligaments. Computational approaches involving finite element (FE) modeling may aid to determine their influence. Previous FE models lacked in precise ligament geometries and material properties, which might have influence on the results. PURPOSE AND STUDY DESIGN: The aim of this study is to investigate ligamentous influence in pelvic stability by means of FE using precise ligament material properties and morphometries. METHODS: An FE model of the pelvis bones was created from computer tomography, including the pubic symphysis joint (PSJ) and the SIJ. Ligament data were used from 55 body donors: anterior (ASL), interosseous (ISL), and posterior (PSL) sacroiliac ligaments; iliolumbar (IL), inguinal (IN), pubic (PL), sacrospinous (SS), and sacrotuberous (ST) ligaments; and obturator membrane (OM). Stress-strain data were gained from iliotibial tract specimens. A vertical load of 600 N was applied. Pelvic motion related to altered ligament and cartilage stiffness was determined in a range of 50% to 200%. Ligament strain was investigated in the standing and sitting positions. RESULTS: Tensile and compressive stresses were found at the SIJ and the PSJ. The center of sacral motion was at the level of the second sacral vertebra. At the acetabula and the PSJ, higher ligament and cartilage stiffnesses decrease pelvic motion in the following order: SIJ cartilageOISLOSTþSSOILþASLþPSL. Similar effects were found for the sacrum (SIJ cartilage OISLOILþASLþPSL) but increased STþSS stiffnesses increased sacral motion. The influence of the IN, OM, and PL was less than 0.1%. Compared with standing, total ligament strain was reduced to 90%. Increased strains were found for the IL, ISL, and PSL. CONCLUSIONS: Posterior pelvic ring cartilage and ligaments significantly contribute to pelvic stability. Their effects are region- and stiffness dependent. While sitting, load concentrations occur at the IL, ISL, and PSL, which goes in coherence with the clinical findings of these ligaments serving as generators of low back pain. Ó 2013 Elsevier Inc. All rights reserved.
Keywords:
Biomechanics; Finite elements modeling; Iliolumbar ligament; Sacroiliac joint ligaments; Sacrospinous and sacrotuberous ligament
FDA device/drug status: Not applicable. Author disclosures: NH: Speaking/Teaching Arrangements: Teaching Anatomy (Salary as Research Assistant and Teacher, government paid); Fellowship Support: Yokochi and Kanehara Fund (Travel allowance and scholarship for cooperation with Japan, C USD). HS: Nothing to disclose. UL: Nothing to disclose. IB: Nothing to disclose. CJ: Nothing to disclose. VS: Speaking/Teaching Arrangements: Ingenium Education Austria (C); Research Support (Investigator Salary): Deutsche Forschungsgemeinsch aft (amount received for staff) (D); Research Support (Staff/Materials): 1529-9430/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.spinee.2013.03.050
Deutsche Forschungsgemeinsch aft (amount received for staff) (D). JB: Nothing to disclose. The disclosure key can be found on the Table of Contents and at www. TheSpineJournalOnline.com. NH and HS contributed equally to the manuscript. * Corresponding author. Faculty of Medicine, Institute of Anatomy, University of Leipzig, Liebigstraße 13, 04103 Leipzig, Germany. Tel.: (49) 341-97-22053; fax: (49) 341-97-22009. E-mail address: [email protected] (N. Hammer)
2
N. Hammer et al. / The Spine Journal
Introduction The influence of posterior pelvic ring ligaments on stability of the pelvis is discussed controversially. Low back pain and sacroiliac joint (SIJ) pain are commonly accepted to be related to pelvic ligament dysfunction [1,2]. The involvement of nociceptive neural elements located within the SIJ region underlines the involvement of ligaments as potential pain generators [3–5]. A significant influence of the sacroiliac ligaments (anterior [ASL], interosseous [ISL], and posterior [PSL] sacroiliac ligaments) was determined in the previous material testing [6–11]. Yet, little or no influence was found for the iliolumbar (IL), sacrospinous (SS), or sacrotuberous ligaments (ST) [6,10,11]. These findings are in contrast with anatomic studies [12–14], biomechanical studies [7,9,15], and with the widely accepted postulate that form and function cohere closely [16,17]. Assuming the biomechanical nonentity in regard to pelvic ligaments, surgical approaches were developed to transect the ligaments in nerve entrapment syndromes [18,19]. In pelvic trauma, pelvic ligaments are still underestimated in radiological and clinical diagnosis and in surgical treatment despite of the poor outcome after anatomic bone reconstruction [20–22]. This lack of consideration of pelvic ligaments may not only be caused by inadequate imaging techniques but also be related to insufficient, sparse information on the pelvic ligaments. Conclusively, questions concerning the function of the pelvic ligaments and their contribution to pelvic stability are unanswered until today. Computational approaches involving finite element (FE) modeling may aid to answer these still open questions. Yet, recent studies using FE lacked in precise geometries and material properties of the pelvic ligaments [23–28]. Additionally, existing results did not suffice to provide quantitative data, especially in concerns of the IL, SS, and ST [29]. New computational models are to be developed, focusing on ligaments to answer these still open
-
(2013)
-
questions about their influence in pelvic stability. This is the main issue of our study, including detailed morphometries of the posterior pelvic ring ligaments. The following hypotheses were addressed: A. An alteration of pelvic ligament or cartilage stiffness properties alters the extent of pelvic motion, proving their influence in stabilization. B. The SS and the ST ligaments significantly contribute to ligamentous effects of pelvic stabilization. C. Pelvic load distribution is different in the standing and sitting positions. Materials and methods Model construction: bones Bone geometry was based on computed tomography (CT) slices of a healthy male pelvis, using 1-mm slices of the pelvic ring [30,31]. Dicom data of both coxal bones and the sacrum of the body donor were imported to Ansys Workbench 12.0 (Ansys, Inc., Canonsburg, PA, USA; Fig. 1). Meshing was accomplished using the virtual topology feature and the patch-independent method for geometry-dependent mesh density [32,33]. The bones were meshed using tetrahedral (Solid187) elements, each consisting of 10 nodes. Material properties of cortical shell were assigned according to the previous literature [34] (Young modulus of elasticity E511,000 N/mm2, shear modulus m50.2). As a simplification, bone isotropy was presumed. Model construction: ligaments The following ligaments of the posterior pelvic ring were included (three-dimensional anatomic shapes): IL (cuboid), ASL (parallelepipeds), ISL (parallelepipeds), PSL (parallelepipeds), SS (frustum), and ST (bifrustum).
Fig. 1. Import of geometries and modeling of the sacroiliac joint (SIJ) Dicom data of both coxal bones (C) and the sacrum (S) were imported to Ansys Workbench 12.0 (Ansys, Inc., Canonsburg, PA, USA). (Left) The anterior view of the meshed bones and (Right) the lateral view at the sacral part of the left SIJ. P, promontory; a, anterior; cd, caudal; cr, cranial; l, left; p, posterior; r, right; scale bar550 mm (left), 25 mm (right).
N. Hammer et al. / The Spine Journal
Ligament morphometry was based on gender-dependent data gained from the anatomic dissection of 55 body donors and CT, 7-T magnetic resonance imaging, and corresponding thin slice plastination of another three body donors [35–37]. Ligament lengths, widths, heights, angles, origin and insertion areas, and fiber orientations were included. Additionally, the obturator membrane and the inguinal and the pubic ligaments were included [38,39]. Meshing was accomplished, using link elements (Fig. 1, Table 1; Link180, large displacement, tension only). Two remote points were defined for each link element, representing one of the main fiber directions within the ligament with the given morphometry. Because of lacking data on pelvic ligament tensile properties, we used the previously published data of the iliotibial tract [40] (E5397 N/mm2). Model construction: joints The SIJ was modeled as a partitioned volume. The ventral cartilaginous part consisted of the auricular surface. The dorsal ligamentous part consisted of the ISL with the given geometry [29,37] (Fig. 2). The pubic symphysis joint (PSJ) was modeled using the published data [38,39]. Material properties of cartilage were assigned for the ventral part of the SIJ and for PSJ according to Guess et al. [41] (E5150 N/mm2, m50.2). Boundary conditions A pelvic inclination of 60 was presumed to simulate gravity effects on the pelvis in the standing position [42,43]. For horizontal loads of the pelvis, a femoral caputcollum-diaphyseal angle of 121 was assumed [44]. The sacrum was defined as a fixed bearing. Because of the missing fifth lumbar vertebra, the origin of the IL was set as a boundary condition with fixed coordinates. The total pelvic load was chosen to be 600 N, equally distributed to both acetabula. Table 1 Ligament load distribution in the standing and the sitting positions Load distribution (%) Ligament
Number of elements
Standing
Sitting
IN PL OM IL ASL ISL PSL SS ST
1 2 1 2 9 5 9 3 3
0.00 0.00 0.12 14.72 12.95 3.57 1.09 39.42 28.12
0.00 0.00 0.12 15.02 12.85 3.75 1.14 39.22 27.90
ASL, anterior sacroiliac ligament; IN, inguinal; PL, pubic; SS, sacrospinous; ST, sacrotuberous ligament; OM, obturator membrane; IL, iliolumbar; ISL, interosseous sacroiliac ligament; and PSL, posterior sacroiliac ligament. Note: The number of elements used for the finite element simulation and relative ligament strain distribution (%) is given for the pelvic ligaments in the standing and the sitting positions. While total pelvic load decreased, strain concentrations were found for the IL, ISL, and PSL.
-
(2013)
-
3
Outcome variables Ten computational substeps were used in the investigation of each outcome variable. The use of each substep served as a verification of material deformation, checking the accuracy of the stiffness matrix and the osteoligamentous model for plausibility: 1. Pelvic motion related to load application was examined. 2. Load distribution of the PSJ and of the SIJ was evaluated graphically by means of a vector presentation. 3. The influence of pelvic ligament and SIJ cartilage material properties to pelvic motion was analyzed. Pelvic ligaments were grouped as follows: inguinal and pubic ligaments, ISL, ILþASLþPSL, and SSþST. Three points were examined at the bony pelvis, averaging the values of both sides if applicable: PSJ (cranial tip), sacral base, and point of load application at the acetabulum. Ligament and cartilage material properties were altered in a range of 50% to 200% (75 N/mm2#Ecartilage#300 N/mm2; 198 N/mm2#Eligament#794 N/mm2}. 4. Relative ligament strain in the sitting and the standing positions was finally computed. Pelvic inclination and femoral tilt were adapted to both load scenarios [45]. The outcome variables of (1) to (3) were calculated in Ansys workbench. The load scenarios were computed in Ansys classic, using Ansys Parametric Design Language. Model validation Load-deformation data were recorded from seven male unembalmed hemipelves (Table 2, mean age 81.576 10.75 years) [29,46]. While alive, the body donors gave informed consent to the donation of their bodies for scientific and educational purposes. The hemipelves were attached to a steel plate with three 8-mm steel screws: one was fixed to the spine at fifth lumbar vertebra and two were fixed to the fourth and fifth sacral vertebrae. An LFEM 600/100/10 material testing machine (WalterþBai, L€ohningen, Switzerland) was used, applying a maximum load of 260 N to the acetabulum by means of a hip joint prosthesis (ABG II H€uftsystem; Stryker GmbH & Co. KG, Duisburg, Germany). Pelvic motion was recorded at the cranial tip of the PSJ and at the acetabulum, using type W10TK displacement transducers, MGL Plus amplifiers, and the Catman software (Hottinger Baldwin Messtechnik GmbH, Darmstadt, Germany). The data of the materials testing were compared with the results of the FE simulation at the following points: ilium (posterior superior iliac spine), acetabulum, and PSJ. Results The pelvic model consisting of the coxal bones, the sacrum, and adjacent ligaments was constructed, using
4
N. Hammer et al. / The Spine Journal
-
(2013)
-
Fig. 2. Modeling of pelvic ligaments. The pelvic ligaments were modeled as link elements, based on precise measurements. The ventral (A), lateral (B), dorsal (C), and cranial (D) views are shown. ASL, anterior sacroiliac ligament; IL, iliolumbar; IN, inguinal; OM, obturator membrane; PL, pubic ligament; PSL, posterior sacroiliac ligament; SS, sacrospinous ligament; ST, sacrotuberous ligament; a, anterior; cd, caudal; cr, cranial; l, left; p, posterior; r, right; scale bar550 mm (A–C), 70 mm (D).
approximately 155,000 elements. A total of 66 link elements were used for all ligaments and the OM (Figs. 1 and 2). Pelvic motion related to load application Applying a vertical load to both acetabula, total PSJ motion was 0.47 mm (Fig. 3). The sacral promontory rotated Table 2 Body donors
caudally and ventrally and the apex of the sacrum rotated cranially and dorsally. Sacral rotation was limited by the SS and ST. The center of rotation is located at the level of second sacral vertebra, depicted as the region of least motion. Both iliac crests were more distant from the sacrum in the loaded condition, compared with the unloaded condition. Load distribution at the PSJ and SIJ
Specimen
Age (y)
Pelvis side
1 2 3 4 5 6 7 Mean6SD
60 75 83 87 88 88 90 81.57
Left Left Left Left Left Right Left 10.75
SD, standard deviation. Note: The age of the body donors is given along with the hemipelvis side used for biomechanical validation.
At the PSJ, tensile stress was found at the cranial and ventral aspect of the pubic arch (Fig. 4, Left, red vectors). More dorsally and caudally at the PSJ, compressive stress was observed (blue). The intermediate region is characterized by both compressive and tensile stresses with different vectors, resulting in bending stress (green vectors, Fig. 4, Left and Middle). Fig. 4, Right, shows the load distribution at the SIJ. Compressive stress was found ventrally in the region of the auricular surface covered with cartilage. Dorsally, tensile stress was observed in the ligament region. Tensile stress was concentrated in the
N. Hammer et al. / The Spine Journal
-
(2013)
-
5
Fig. 3. Load-displacement results of the osteoligamentous finite element model, depicted in red (left). Maximum displacements were measured at the pubic symphysis with 0.47 mm, depicted in red. The promontory (P) rotated caudally and ventrally. The center sacral motion is at the level of the second sacral vertebra, depicted in blue (right). C, coxal bone; S, sacrum; a, anterior; cd, caudal; cr, cranial; l, left; p, posterior; r, right; scale bar550 mm.
dorsal and cranial SIJ compartment with the ISL and PSL. At level of the second sacral vertebra (center of rotation), least compressive and tensile stresses were observed. The influence of ligament and cartilage material properties in pelvic motion An increase of SIJ cartilage and ligament material stiffnesses decreased pelvic motion at all the observed points
with one exception: higher SSþST stiffnesses increased sacral motion. The results are given in Fig. 5. The following order was observed regarding the magnitude of motion, caused by altered ligament and cartilage properties: at the PSJ and acetabulum, alteration of SIJ cartilage stiffnesses had most influence, followed by ISL, SSþST, and ILþASLþPSL, and at the sacral base, SSþST’ stiffness had most influence, followed by SIJ cartilage, ISL, and ILþASLþPSL. Alteration of inguinal and pubic ligaments’
Fig. 4. Load distribution at the pubic symphysis joint (PSJ) and sacroiliac joint (SIJ). The SIJ (Left, lateral view) is characterized by compression in the ventral (cartilaginous) region and by tension in the dorsal ligamentous region. Least stress-strain was observed at the level of the second sacral vertebra, and strain concentration was located in the cranial and dorsal regions of the iliolumbar, the interosseous, and posterior sacroiliac ligaments, indicated by red arrows. At the PSJ (Middle, ventral view; Right, lateral view), compression was observed dorsally and caudally. The intermediate and cranial regions are characterized by both compression and tension with different vectors, resulting in bending stress. a, anterior; cd, caudal; cr, cranial; l, left; p, posterior; r, right; blue vectors: compressive force; red vectors: strain; green vectors: torsional/bending stress; scale bar515 mm (Left), 4 mm (Middle and Right).
6
N. Hammer et al. / The Spine Journal
-
(2013)
-
Model validation In the comparison of the load-deformation data of the hemipelves with the FE model at the given points, displacement directions matched (Fig. 6). Pelvic deformation of the body donors was one magnitude larger.
Discussion Biomechanical and clinical observations
Fig. 5. Influence of cartilage and ligament properties on the extent of pelvic motion. An increase of SIJ cartilage and ligament material stiffnesses decreased pelvic motion at all the observed points (Top, Middle, and Bottom) with one exception: higher STþSS stiffnesses increased sacral motion (Top). SS, sacrospinous; ST, sacrotuberous ligament; PL, pubic ligament; OM, obturator membrane; IL, iliolumbar; ASL, anterior sacroiliac ligament; PSL, posterior sacroiliac ligament; IN, inguinal; ISL, interosseous sacroiliac ligament; SIJ, sacroiliac joint.
stiffnesses resulted in least alteration of motion at all the observed points (O0.1%). Relative ligament strain in the sitting and the standing positions The resulting vectors applied to both acetabula were x5180.26 N, y5150.00 N, and z5259.81 N for the standing position (pelvic inclination560 ) and x5180.23 N, y5251.60 N, and z5163.39 N for the sitting position (pelvic inclination533 ). In contrast, ligament strain increased within the IL, ISL, and PSL (Table 1).
In accordance to the previous literature [7,15,47], the stabilizing function of the ASL, ISL, and PSL was confirmed by recent biomechanical tests [10,11,46,48] and with our virtual setup. Scolumb and Terry [15], Miller et al. [48], and Rothk€otter and Berner [8] recorded the load-displacement behavior and the failure characteristics of the SIJ in biomechanical testing of a large number of specimens. Yet, no distinction of the ISL and PSL could be made with regard to their individual influence in pelvic stability. Little influence was found for the IL, SS, and ST as stabilizers [6,10,11], which mismatched with other findings [49–52]. Based on this ‘‘lack of function,’’ surgical transection of the SS and ST was developed for the pudendal nerve entrapment syndrome [18,19]. The major limitation of the studies of Philippeau et al. [18] and Vrahas et al. [10] was that they exclusively performed material testing with axial loads of the SIJ, neglecting the multiaxial nature of the SIJ and its nutation movement [12]. In a similar manner, Vukicevic et al. [11] applied double sandwich interferometry in a setup that prevented the pelvis from tilting. Doing so, the SS and ST possibly remained unloaded [10,11,18]. Conza et al. [6] applied one dimensional laser vibrometry in a range of 10 to 340 Hz in one specimen and determined no influence of the IL, SS, and ST in pelvic stability. Their conclusions can be rebutted by PoolGoudzwaard et al. [51] in mechanical tests of 12 donors and by our findings. Also, Neugebauer et al. [53] found out that the pelvis is best characterized at frequencies between 500 and 2,000 Hz using three-dimensional laser vibrometries in a much larger specimen number than Conza et al. [6]. Proving hypotheses (A) and (B), our study confirms significant influence of all posterior pelvic ring ligaments on stabilization—including the IL, SS, and ST. Alteration of pelvic motion was observed, related to altered ligament and cartilage properties. At the acetabula and the PSJ, SIJ cartilage properties mostly reduce motion, followed by the SS and ST, the ISL, and the group of IL, ASL, and PSL properties. At the sacrum, SIJ cartilage reduces pelvic motion to the largest extent, followed by the ISL and the group of IL, ASL, and PSL. An opposite effect was determined for the SS and ST: increased stiffnesses caused increased sacral motion. This is reasonable, when looking at the boundary conditions that defined the top of the
N. Hammer et al. / The Spine Journal
-
(2013)
-
7
force transmission with subsequent axial rotation and translation. At the SIJ, the lever ratio of the SS and ST is more effective, compared with the ISL with a larger crosssectional area [37]. Because of these effects, the influence of the SS and ST is weakened at the acetabula and the PSJ. Here, the lever arms of the SIJ cartilage and ISL are more effective. The inguinal and pubic ligaments had least influence on alteration of pelvic motion, which might be the result of cumulative effects to neutralize stresses at the PSJ [38,39]. In our graphical evaluation (Fig. 3), the center of axial rotation was determined within the ISL at level of second sacral vertebra, which complies with previous studies [54] and the previous description of the ISL as Achsenband [55,56]. Compressive, tensile, and shear forces were found for the PSJ and SIJ, which confirms biomechanical [38,39] and histologic findings [12,57,58]. Alterations in cartilage material properties, for example related to arthritis or arthrosis elsewhere [59], significantly affect pelvic motion. In accordance with hypothesis (C), alterations of load distributions were found for the sitting position, compared with standing. Local strain concentrations were determined at the IL, ISL, and PSL. These findings confirm that nerve endings located within the SIJ and IL ligaments [9,60–62] may serve as generators of low back pain during ligament strain [51,63]. This effect can be increased in the sitting position or by so-called slouching movements [64]. Comparison with other FE simulations
Fig. 6. Comparison of load-deformation data of the hemipelves with the finite element (FE) model. In the validation with the body donors, displacement directions matched. The ilium (Top, posterior superior iliac spine), acetabulum (Middle), and pubic symphysis joint (Bottom) were observed. Deformations of the body donors (circles) were one magnitude larger, compared with the FE simulation (triangles).
sacrum as a fixed support. The influence can be explained by the geometry and the cross-sectional areas of the aforementioned ligaments [14,15,40,47]. The SS and ST directly connect the ischium to the distal sacrum, causing direct
Few FE studies on posterior pelvic ring ligaments are available in literature. These studies were based on hemipelves [23,24,26], fixed SIJ [25], or on limited ligament data [24,27–29,65]. Investigators of posterior pelvic ring morphometries faced two problems: first, the ligaments situated inside the SIJ could not be measured sufficiently and were, therefore, estimated [14,66,67] and second, measurements of a small number of specimens may neither represent the standard case nor allow using gender-dependent data [68–70]. Third, previous measurements were optimized for anthropological purposes, not for virtual biomechanics. Geometries of ligaments influence the results of biomechanical and virtual simulations [71]. We previously determined anatomic data of the posterior pelvic ring ligament geometries for the given FE model [35–37]. Anatomic preparations and frozen sections were accomplished in pelves of 55 body donors along with correlating CT, 7-T magnetic resonance imaging, and thin slice plastination in another 3 donors. Using these techniques, an in situ visualization and description of the ligaments were possible. Another issue to be addressed is the lack of stiffness properties of pelvic ring ligaments. Existing literature only provides load-displacement data of the entire pelvic ring [7,8] or of the isolated SIJ [48]. Because of the complexity of the SIJ ligaments and their anatomic location being surrounded by the sacrum and the coxal bones, their strain data
8
N. Hammer et al. / The Spine Journal
can presently only be estimated. Reliable stress-strain properties of the IL, SS, and ST are presently not available. Some FE simulations included numerically estimated data [25,28,65] or published data of the human knee ligaments [27]. Because these material properties may not be true for the pelvic ligaments, we decided to use iliotibial tract material properties [40]. The tract is none of the ligaments considered in our FE model, but its material data may be more reasonable than knee data because of its topographical proximity and influence on pelvic mechanics. Additionally, its parallel fibers allowed precise measurements. The main results of previous FE studies can be confirmed and extended with our present investigation. The IL, ASL, ISL, and PSL are involved in horizontal load transfer at the acetabulum and ilium [29]. The SS and ST provide vertical load transfer with subsequent translation of the sacrum [29]. These results were now quantified. Eichenseer et al. [27] found that decreasing ligament stiffnesses increase SIJ stress and angular motion with maximum strains at the ISL. This is can be confirmed for all ligaments except for the SS and ST. The latter ligaments increase sacral motion at increasing stiffnesses. Ligament-related differences in stress-strain fields, as observed by Phillips et al. [25], are, therefore, reasonable because of different ligament effects at different locations of the pelvis. Validation and limitations Finite element modeling is a simplification of the functional anatomy of biological tissues. Only structures that have actually been included into the models can be observed with regard to their function. In our present model, no muscles have been integrated. The erector spinae, the quadratus lumborum [72,73], abdominal wall muscles [4,74,75], the gluteus maximus [73,76,77], and further muscles [75,78] were found to exert influence on pelvic ring and the SIJ. Despite this simplification, FE modeling may aid to determine ligament and joint mechanics if standard material testing will not give satisfactory results. This is especially true for the ISL, SS, and ST. Rigid isotropic properties were attributed to the bones, which is a simplification with effects on our validation data with the body donors. Although the direction of motion is equal for all points, in situ motion with body donors is one magnitude higher than computed in our model. Also, hemipelves of body donors are compared with a complete pelvis investigated that might have an effect on the validation. Yet, the maximum pelvic displacement in our model was 0.47 mm at the PSJ (load 600 N), which is comparable with the published data ([48]: 0.28 mm at 294 N, [8]: 0.45 mm at 600 N). The origin at the IL was defined as a fixed boundary condition because of missing data of the fifth lumbar vertebra. Motion of lumbosacral transition was excluded. Being aware of these limitations of the osseous components, ligamentous influence on the pelvic ring could be observed successfully with our model, proving the three hypotheses. Although the
-
(2013)
-
iliotibial tract overspans the pelvis and the hip joint, it might not necessarily reflect the mechanical characteristics of the posterior pelvic ring ligaments but seems to be more justifiable than knee ligaments [27]. Stress-strain data gained from the posterior pelvic ring ligaments will have to be integrated into future models. Models that integrate these data along with muscle loads and anisotropic data of cortical and cancellous bone may be the next step. Further optimization of structural geometry may aid to reduce the error probability and shorten computational time.
Conclusions and outlook This is the first study to determine the influence of posterior pelvic ligaments in pelvic motion, based on detailed morphometries. Posterior pelvic ring cartilage and ligaments significantly contribute to pelvic stability. Ligamentous effects on the bony pelvis are region- and stiffness dependent. The SS and ST significantly contribute to ligament stability of the pelvis. Total ligament strain is larger in the standing position, compared with the sitting position. In the sitting position, load concentrations occur at the IL, ISL, and PSL, which goes in coherence with the clinical findings of these ligaments serving as generators of low back pain [9,64,79]. Further clinical questioning may be answered in regard to low back pain and to surgical treatment of ligaments in pelvic fractures, using osteoligamentous FE models. References [1] Cohen SP. Sacroiliac joint pain: a comprehensive review of anatomy, diagnosis, and treatment. Anesth Analg 2005;101:1440–53. [2] Fortin JD, Vilensky JA, Merkel GJ. Can the sacroiliac joint cause sciatica? Pain Physician 2003;6:269–71. [3] Damen L, Spoor CW, Snijders CJ, Stam HJ. Does a pelvic belt influence sacroiliac joint laxity? Clin Biomech (Bristol, Avon) 2002; 17:495–8. [4] Mens JMA, Damen L, Snijders CJ, Stam HJ. The mechanical effect of a pelvic belt in patients with pregnancy-related pelvic pain. Clin Biomech (Bristol, Avon) 2006;21:122–7. [5] Pel JJM, Spoor CW, Goossens RHM, Pool-Goudzwaard AL. Biomechanical model study of pelvic belt influence on muscle and ligament forces. J Biomech 2008;41:1878–84. [6] Conza NE, Rixen DJ, Plomp S. Vibration testing of a fresh-frozen human pelvis: the role of the pelvic ligaments. J Biomech 2007; 40:1599–605. [7] Fessler J. Die Festigkeit der menschlichen Gelenke mit besonderer Ber€ucksichtigung des Bandapparates. Habilitationsschrift. M€unchen, Germany, 1894. [8] Rothk€otter HJ, Berner W. Failure load and displacement of the human sacroiliac joint under in vitro loading. Arch Orthop Trauma Surg 1988;107:283–7. [9] Varga E, Dudas B, Tile M. Putative proprioceptive function of the pelvic ligaments: biomechanical and histological studies. Injury 2008;39:858–64. [10] Vrahas M, Hern TC, Diangelo D, et al. Ligamentous contributions to pelvic stability. Orthopedics 1995;18:271–4. [11] Vukicevic S, Marusic A, Stavljenic A, et al. Holographic analysis of the human pelvis. Spine 1991;16:209–14.
N. Hammer et al. / The Spine Journal [12] Kapandji IA. Funktionelle Anatomie der Gelenke: Schematisierte und kommentierte Zeichnungen zur menschlichen Biomechanik: einb€andige Ausgabe—obere Extremit€at, untere Extremit€at, Rumpf und Wirbels€aule. 5th ed. Stuttgart, Germany: Thieme, 2009. [13] Tittel K. Beschreibende und funktionelle Anatomie des Menschen. 14th ed. M€ unchen, Germany: Urban & Fischer, 2003. [14] Weisl H. The ligaments of the sacro-iliac joint examined with particular reference to their function. Acta Anat (Basel) 1954;20: 201–13. [15] Scolumb L, Terry R. Influence of the sacrotuberous and sacrospinous ligaments in limited movements of the sacroiliac joint. J Am Med Assoc 1926;87:307–9. [16] Pauwels F. Eine neue Theorie €uber den Einfluss mechanischer Reize auf die Differenzierung der St€utzgewebe. Zehnter Beitrag zur funktionellen Anatomie und kausalen Morphologie des St€utzapparates. Z Anat Entwicklungsgesch 1960;121. [17] Russell ES. Form and function: a contribution to the history of animal morphology. London, UK: Murray, 1916. [18] Philippeau J, Hamel O, Pecot J, Robert R. R^ole biomecanique des ligaments sacroepineux et sacrotuberal sur la stabilite de l’articulation sacro-iliaque. Anatomie et etude experimentale originale. Morphologie 2008;92:16–30. [19] Robert R, Prat-Pradal D, Labat JJ, et al. Anatomic basis of chronic perineal pain: role of the pudendal nerve. Surg Radiol Anat 1998; 20:93–8. [20] Burkhardt M, Culemann U, Seekamp A, Pohlemann T. Operative Versorgungsstrategien beim Polytrauma mit Beckenfraktur. Eine Literatur€ ubersicht. Unfallchirurg 2005;108:812. 814–820. [21] G€ansslen A, Pohlemann T, Paul C, et al. Epidemiology of pelvic ring injuries. Injury 1996;27(1 Suppl):SA13–20. [22] Pohlemann T, Tscherne H, Baumg€artel F, et al. Beckenverletzungen: € €uber die Epidemiologie, Therapie und Langzeitverlauf. Ubersicht multizentrische Studie der Arbeitsgruppe Becken. Unfallchirurg 1996;99:160–7. [23] Dalstra M, Huiskes R, van Erning L. Development and validation of a three-dimensional finite element model of the pelvic bone. J Biomech Eng 1995;117:272–8. [24] Murakami H, Kawahara N, Tomita K, et al. Biomechanical evaluation of reconstructed lumbosacral spine after total sacrectomy. J Orthop Sci 2002;7:658–64. [25] Phillips ATM, Pankaj P, Howie CR, et al. Finite element modelling of the pelvis: inclusion of muscular and ligamentous boundary conditions. Med Eng Phys 2007;29:739–48. [26] Anderson AE, Peters CL, Tuttle BD, Weiss JA. Subject-specific finite element model of the pelvis: development, validation and sensitivity studies. J Biomech Eng 2005;127:364–73. [27] Eichenseer PH, Sybert DR, Cotton JR. A finite element analysis of sacroiliac joint ligaments in response to different loading conditions. Spine 2011;36:E1446–52. [28] Garcıa JM, Doblare M, Seral B, et al. Three-dimensional finite element analysis of several internal and external pelvis fixations. J Biomech Eng 2000;122:516–22. [29] B€ ohme J, Steinke H, H€ulse R, et al. Komplexe ligament€are Instabilit€aten nach "open book"-Verletzungen des Beckenrings— Finite-Elemente-Computersimulation und Bruchversuch. Z Orthop Unfall 2011;149:83–9. [30] Shim VB, Pitto RP, Streicher RM, et al. The use of sparse CT datasets for auto-generating accurate FE models of the femur and pelvis. J Biomech 2007;40:26–35. [31] Shim VB, Pitto RP, Streicher RM, et al. Development and validation of patient-specific finite element models of the hemipelvis generated from a sparse CT data set. J Biomech Eng 2008;130: 51010. [32] Lawrence KL. ANSYS Workbench Tutorial: structural & thermal analysis using the ANSYS workbench release 11.0 environment. Mission, KS: Schroff Development Corp., 2007.
-
(2013)
-
9
[33] Lee H. Finite element simulations with ANSYS workbench 12: theory, applications, case studies. Mission, KS: Schroff Development Corp., 2010. [34] Wirtz DC, Schiffers N, Pandorf T, et al. Critical evaluation of known bone material properties to realize anisotropic FE-simulation of the proximal femur. J Biomech 2000;33:1325–30. [35] Hammer N, Steinke H, B€ohme J, et al. Description of the iliolumbar ligament for computer-assisted reconstruction. Ann Anat 2010;192: 162–7. [36] Hammer N, Steinke H, Slowik V, et al. The sacrotuberous and the sacrospinous ligament—a virtual reconstruction. Ann Anat 2009; 191:417–25. [37] Steinke H, Hammer N, Slowik V, et al. Novel insights into the sacroiliac joint ligaments. Spine 2010;35:257–63. [38] Li Z, Alonso JE, Kim J, et al. Three-dimensional finite element models of the human pubic symphysis with viscohyperelastic soft tissues. Ann Biomed Eng 2006;34:1452–62. [39] Li Z, Kim J, Davidson JS, et al. Biomechanical response of the pubic symphysis in lateral pelvic impacts: a finite element study. J Biomech 2007;40:2758–66. [40] Steinke H, Lingslebe U, B€ohme J, et al. Deformation behavior of the iliotibial tract under different states of fixation. Med Eng Phys 2012; 34:1221–7. [41] Guess TM, Thiagarajan G, Kia M, Mishra M. A subject specific multibody model of the knee with menisci. Med Eng Phys 2010; 32:505–15. [42] Boulay C, Tardieu C, Hecquet J, et al. Sagittal alignment of spine and pelvis regulated by pelvic incidence: standard values and prediction of lordosis. Eur Spine J 2006;15:415–22. [43] Le Demany P. L’angle sacro-pelvien, ses variations professionnelles. J Anat Physiol Norm Pathol Homm Anim 1909;45:276–87. [44] Alverdes K. Grundlagen der Anatomie. 3rd ed. Leipzig, Germany: VEB Georg Thieme, 1956. [45] H€ulse R, Hammer N, Steinke H, et al. Finite Elemente Modell des Beckens zur Simulation komplexer ligament€arer Instabilit€atsszenarien. In: Meinzer HP, Deserno TM, Handels H, Tolxdorff T, eds. Bildverarbeitung f€ur die Medizin 2009: Algorithmen, Systeme, Anwendungen: Proceedings des Workshops vom 22. bis 25. M€arz 2009 in Heidelberg. Berlin, Germany: Springer, 2009: 434–8. [46] Krause M. Experimentelle Untersuchung zum Verformungsverhalten des menschlichen Beckenrings. Leipzig, Germany: Diplomarbeit, 2007. [47] Weber W, Weber E. Die Mechanik der menschlichen Gehwerkzeuge: Eine anatomisch-physiologische Untersuchung. G€ottingen, Germany: Dieterichsche Buchhandlung, 1836. [48] Miller JA, Schultz AB, Andersson GB. Load-displacement behavior of sacroiliac joints. J Orthop Res 1987;5:92–101. [49] Basadonna PT, Gasparini D, Rucco V. Iliolumbar ligament insertions. In vivo anatomic study. Spine 1996;21:2313–6. [50] Hartford JM, McCullen GM, Harris R, Brown CC. The iliolumbar ligament: three-dimensional volume imaging and computer reformatting by magnetic resonance: a technical note. Spine 2000;25: 1098–103. [51] Pool-Goudzwaard A, van Hoek Dijke G, Mulder P, et al. The iliolumbar ligament: its influence on stability of the sacroiliac joint. Clin Biomech (Bristol, Avon) 2003;18:99–105. [52] Sims JA, Moorman SJ. The role of the iliolumbar ligament in low back pain. Med Hypotheses 1996;46:511–5. [53] Neugebauer R, Werner M, Voigt C, et al. Experimental modal analysis on fresh-frozen human hemipelvic bones employing a 3D laser vibrometer for the purpose of modal parameter identification. J Biomech 2011;44:1610–3. [54] Puhakka KB, Melsen F, Jurik AG, et al. MR imaging of the normal sacroiliac joint with correlation to histology. Skeletal Radiol 2004; 33:15–28.
10
N. Hammer et al. / The Spine Journal
[55] Farabeuf L. Sur l’anatomie et la physiologie des articulations sacroiliaques avant et apres la symphyseotomie. Gynecol Obstet (Paris) 1894;41:407–20. [56] Klein G. Zur Mechanik des Ileosacralgelenkes. Ann Anat 1891;6: 74–118. [57] Bennemann R. Untersuchungen am Iliosakralgelenk des Menschen. Verh Anat Ges 1979;73:187–90. [58] Tillmann B. Funktionelle Anpassung an Gelenken mit unterschiedlichem Belastungsmodus. Langenbecks Arch Chir Suppl II Verh Dtsch Ges Chir 1989;459–64. [59] G€ orke U, G€ unther H, Nagel T, Wimmer MA. A large strain material model for soft tissues with functionally graded properties. J Biomech Eng 2010;132:74502. [60] Bogduk N, Macintosh JE. The applied anatomy of the thoracolumbar fascia. Spine 1984;9:164–70. [61] Kellgren J. On the distribution of pain arising from deep somatic structures with charts of segmental pain areas. Clin Sci 1939;4: 35–46. [62] Szadek KM, Hoogland PVJM, Zuurmond WW, et al. Possible nociceptive structures in the sacroiliac joint cartilage: an immunohistochemical study. Clin Anat 2010;23:192–8. [63] Snijders CJ, Hermans PFG, Niesing R, et al. The influence of slouching and lumbar support on iliolumbar ligaments, intervertebral discs and sacroiliac joints. Clin Biomech (Bristol, Avon) 2004;19:323–9. [64] Snijders CJ, Hermans PFG, Niesing R, et al. Effects of slouching and muscle contraction on the strain of the iliolumbar ligament. Man Ther 2008;13:325–33. [65] Zheng N, Watson LG, Yong-Hing K. Biomechanical modelling of the human sacroiliac joint. Med Biol Eng Comput 1997;35:77–82. [66] Attias N, Arzani S, Duncan G, et al. Sectional imaging anatomy: pelvic ring ligaments. J Comput Assist Tomogr 2001;25:975–9. [67] Rosatelli AL, Agur AM, Chhaya S. Anatomy of the interosseous region of the sacroiliac joint. J Orthop Sports Phys Ther 2006;36: 200–8. [68] Gerlach UJ, Lierse W. Functional construction of the sacroiliac ligamentous. Acta Anat (Basel) 1992;144:97–102.
-
(2013)
-
[69] Remy M, Bouillet P, Bertin P, et al. Evaluation of magnetic resonance imaging for the detection of sacroiliitis in patients with early seronegative spondylarthropathy. Rev Rhum Engl Ed 1996;63: 577–83. [70] Seizeur R, Forlodou P, Person H, et al. The morphometric study of the sacrospinal and sacrotuberal ligaments correlated with the morphometry of the pelvis. Surg Radiol Anat 2005;27:517–23. [71] Lanovaz JL, Ellis RE. A cadaverically evaluated dynamic FEM model of closed-chain TKR mechanics. J Biomech Eng 2009;131:51002. [72] Park K, Kim S, Oh D. Effects of the pelvic compression belt on gluteus medius, quadratus lumborum, and lumbar multifidus activities during side-lying hip abduction. J Electromyogr Kinesiol 2010;20: 1141–5. [73] Takasaki H, Iizawa T, Hall T, et al. The influence of increasing sacroiliac joint force closure on the hip and lumbar spine extensor muscle firing pattern. Man Ther 2009;14:484–9. [74] Beales DJ, O’Sullivan PB, Briffa NK. The effects of manual pelvic compression on trunk motor control during an active straight leg raise in chronic pelvic girdle pain subjects. Man Ther 2010;15:190–9. [75] Hu H, Meijer OG, van Die€en JH, et al. Muscle activity during the active straight leg raise (ASLR), and the effects of a pelvic belt on the ASLR and on treadmill walking. J Biomech 2010;43:532–9. [76] Arumugam A, Milosavljevic S, Woodley S, Sole G. Effects of external pelvic compression on form closure, force closure, and neuromotor control of the lumbopelvic spine—a systematic review. Man Ther 2012;17:275–84. [77] Massoud Arab A, Reza Nourbakhsh M, Mohammadifar A. The relationship between hamstring length and gluteal muscle strength in individuals with sacroiliac joint dysfunction. J Man Manip Ther 2011;19:5–10. [78] Jung H, Jeon H, Oh D, Kwon O. Effect of the pelvic compression belt on the hip extensor activation patterns of sacroiliac joint pain patients during one-leg standing: a pilot study. 2012 Oct 27. [Epub ahead of print]. http://dx.doi.org/10.1016/j.math.2012.09.003. [79] Vleeming A, Stoeckart R, Volkers AC, Snijders CJ. Relation between form and function in the sacroiliac joint. Part I: clinical anatomical aspects. Spine 1990;15:130–2.