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Spondylophyte classification based on biomechanical effects on segmental stiffness

Open AccessPublished:June 04, 2022DOI:https://doi.org/10.1016/j.spinee.2022.06.001

      Highlights

      • Location and cranio-caudal extent of spondylophytes are essential parameters for their biomechanical effect.
      • The largest biomechanical effect of non-bridging spondylophytes is during contralateral bending.
      • Computed tomography images provide substantial interreader agreement for the grading of the cranio-caudal extent of spondylophytes.

      Abstract

      BACKGROUND CONTEXT

      The biomechanical impact of spondylophytes on segmental stiffness is largely unknown, despite their high incidence.

      PURPOSE

      The aim of this study was to quantify the biomechanical contribution according to location and cranio-caudal extent of spondylophytes and to create a clinically applicable radiological classification system.

      STUDY DESIGN

      Biomechanical cadaveric study.

      METHODS

      Twenty-six cadaveric human lumbar spinal segments with spondylophytes were tested with a displacement-controlled stepwise reduction method. The reduction in load required for the same motion after spondylophyte dissection was used to calculate the biomechanical contribution in flexion, extension, axial rotation, lateral bending, anterior, posterior and lateral shear. The spondylophytes were categorized by assessment of their anatomical position and cranio-caudal extent in computed tomography images (grade 1: spondylophytes spanning less than 50% of the disc-height, grade 2:>50%, grade 3:>90%, grade 4: bony bridging between the vertebrae) by two experienced radiologists. Cohen's kappa (κ) was used to report interreader reliability.

      RESULTS

      The largest biomechanical effect of non-bridging spondylophytes (grade 1–3) was recorded during contralateral bending with a grade-dependent contribution of up to 35%. Other loading directions including ipsilateral bending and translational loading were affected with values below 13%. Spondylophytes with osseous bridging (grade 4) show large contribution to the segmental stiffness in most loading conditions with values reaching over 80%. Interreader agreement for the spondylophyte grading was “substantial” (κ=0.73, p<.001).

      CONCLUSIONS

      The location and cranio-caudal extent of spondylophytes are essential parameters for their biomechanical effect. A reproducible classification has been validated biomechanically and helps evaluate the effect of specific spondylophyte configurations on segmental stiffness.

      CLINICAL SIGNIFICANCE

      Non-bridging spondylophytes primarily act as tensile structures and do not provide relevant propping. A classification system is presented to support understanding of the biomechanical consequences of different spondylophyte configuration for clinical decision making in surgical planning.

      Keywords

      Introduction

      Vertebral osteophytes, so called spondylophytes, are defined as abnormal bony growth at the rim of the vertebral bodies [
      • Boos N
      • Aebi M.
      Spinal disorders: fundamentals of diagnosis and treatment.
      ,
      • Klaassen Z
      • Tubbs RS
      • Apaydin N
      • Hage R
      • Jordan R
      • Loukas M.
      Vertebral spinal osteophytes.
      ,
      • Quinnell RC
      • Stockdale HR.
      The significance of osteophytes on lumbar vertebral bodies in relation to discographic findings.
      ]. The term spondylophyte is derived from the Greek words spondylos for spine, and phytein for to grow [
      • Boos N
      • Aebi M.
      Spinal disorders: fundamentals of diagnosis and treatment.
      ]. Spondylophytes show high incidence in the general population. Their formation has been observed to start at the age of 20, while at the age of 40, small spondylophytes are present in the majority of the population and at the age of 80, severe spondylophytes are present in close to all patients [
      • Nathan H.
      Osteophytes of the vertebral column.
      ]. Despite the large incidence, the etiology as well as the biomechanical role of spondylophytes is not well understood [
      • De Schepper EIT
      • Damen J
      • Van Meurs JBJ
      • Ginai AZ
      • Popham M
      • Hofman A
      • et al.
      The association between lumbar disc degeneration and low back pain: the influence of age, gender, and individual radiographic features.
      ,
      • Huyghe JM
      • Wilke H-J
      • Galbusera F
      • Ito K
      • van Rijsbergen M
      • Brayda-Bruno M.
      Ageing and degenerative changes of the intervertebral disc and their impact on spinal flexibility.
      ]. Histologic evaluation indicates spondylophytes to be the result of endochondral ossification [
      • Padur AA
      • Kumar N
      • Shanthakumar SR
      • Bishnu A.
      Morphometric and histological study of osteophytes in human cadaveric lumbar vertebrae.
      ]. Spondylophytes are located mostly at the anterior and anterolateral border of the vertebrae, while a dorsal location is markedly less frequent [
      • Nathan H.
      Osteophytes of the vertebral column.
      ]. Morphologically different types of spondylophytes were described [
      • Harris RI
      • Macnab I.
      Structural changes in the lumbar intervertebral discs; their relationship to low back pain and sciatica.
      ], with the most common type being hypothesized to play a role as a propping structure due to its claw-like appearance. On the other side, the so-called traction spurs (horizontal spondylophytes) were postulated to be triggered by segmental instability and were assumed to be an active mechanism of the body to stabilize the segment [
      • Macnab I.
      The traction spur. an indicator of segmental instability.
      ,
      • Yadav SS.
      Traction spur.
      ]. While slightly different distribution patterns for claw-type and traction-spondylophytes were noted [
      • Kasai Y
      • Kawakita E
      • Sakakibara T
      • Akeda K
      • Uchida A.
      Direction of the formation of anterior lumbar vertebral osteophytes.
      ], combined occurrence in a single segment, intermediate types as well as changes in type were described [
      • Pate D
      • Goobar J
      • Resnick D
      • Haghighi P
      • Sartoris DJ
      • Pathria MN.
      Traction osteophytes of the lumbar spine: radiographic-pathologic correlation.
      ,
      • Heggeness MH
      • Doherty BJ.
      Morphologic study of lumbar vertebral osteophytes.
      ]. With the absence of histologic differences [
      • Pate D
      • Goobar J
      • Resnick D
      • Haghighi P
      • Sartoris DJ
      • Pathria MN.
      Traction osteophytes of the lumbar spine: radiographic-pathologic correlation.
      ], a growing consensus emerged that the morphologically of different spondylophytes do not represent different pathologies but rather different stages of the same process [
      • Quinnell RC
      • Stockdale HR.
      The significance of osteophytes on lumbar vertebral bodies in relation to discographic findings.
      ,
      • Pate D
      • Goobar J
      • Resnick D
      • Haghighi P
      • Sartoris DJ
      • Pathria MN.
      Traction osteophytes of the lumbar spine: radiographic-pathologic correlation.
      ]. With the position of the aorta affecting the location of spondylophyte formation [
      • Nathan H.
      Osteophytes of the vertebral column.
      ] and with osteoporosis being associated with lower spondylophyte incidence [
      • Miyakoshi N
      • Itoi E
      • Murai H
      • Wakabayashi I
      • Ito H
      • Minato T.
      Inverse relation between osteoporosis and spondylosis in postmenopausal women as evaluated by bone mineral density and semiquantitative scoring of spinal degeneration.
      ], local and metabolic factors appear to play a role in spondylophyte formation as well. Degenerative changes such as endplate sclerosis [
      • Pye SRR
      • Reid DMM
      • Lunt M
      • Adams JEE
      • Silman AJJ
      • O'Neill TWW
      Lumbar disc degeneration: association between osteophytes, end-plate sclerosis and disc space narrowing.
      ], disc calcification [
      • Chanchairujira K
      • Chung CBB
      • Kim JYY
      • Papakonstantinou O
      • Lee MHH
      • Clopton P
      • et al.
      Intervertebral disk calcification of the spine in an elderly population: radiographic prevalence, location, and distribution and correlation with spinal degeneration.
      ] and disc space narrowing [
      • Pye SRR
      • Reid DMM
      • Lunt M
      • Adams JEE
      • Silman AJJ
      • O'Neill TWW
      Lumbar disc degeneration: association between osteophytes, end-plate sclerosis and disc space narrowing.
      ] are correlated with spondylophyte occurrence and could also influence their formation. However, the presence of spondylophytes in non-degenerated segments contradicts the assumption of spondylophytes being solely induced by degenerative processes [
      • Quinnell RC
      • Stockdale HR.
      The significance of osteophytes on lumbar vertebral bodies in relation to discographic findings.
      ,
      • Oishi Y
      • Shimizu K
      • Katoh T
      • Nakao H
      • Yamaura M
      • Furuko T
      • et al.
      Lack of association between lumbar disc degeneration and osteophyte formation in elderly Japanese women with back pain.
      ].
      The hypothesis, that spondylophytes are an adaptive process to compressive overloading and act as a propping structure is supported by the predominance of spondylophytes at locations with high axial loading: Highest prevalence of anterior spondylophytes at the kyphotic apex of the thoracic spine and the highest relative occurrence of dorsal osteophytes at the lordotic apexes of the cervical and lumbar spine [
      • Nathan H.
      Osteophytes of the vertebral column.
      ]. Similarly, spondylophytes occur more frequently in the concavity of scoliotic curves [
      • Nathan H.
      Osteophytes of the vertebral column.
      ] and bipedal rats show a higher spondylophyte-frequency than quadruped controls [
      • Gloobe H
      • Nathan H.
      Osteophyte formation in experimental bipedal rats.
      ]. Spondylophytes also occur more frequently in people with higher body-mass-index (BMI) [
      • Oishi Y
      • Shimizu K
      • Katoh T
      • Nakao H
      • Yamaura M
      • Furuko T
      • et al.
      Lack of association between lumbar disc degeneration and osteophyte formation in elderly Japanese women with back pain.
      ,
      • Cvijetić S
      • McCloskey E
      • Koršić M.
      Vertebral osteophytosis and vertebral deformities in an elderly population sample.
      ] and in patients with spinal deformities [
      • Cvijetić S
      • McCloskey E
      • Koršić M.
      Vertebral osteophytosis and vertebral deformities in an elderly population sample.
      ].
      The hypothesis, that spondylophytes could be an adaptive process to prevent segmental instability [
      • Macnab I.
      The traction spur. an indicator of segmental instability.
      ,
      • Yadav SS.
      Traction spur.
      ], has not been supported by further research, however the biomechanical role of spondylophytes during translational loads is largely unknown.
      However, spondylophytes are not limited to locations of high compressive stresses or segmental instability and also occur in quadruped animals [
      • Morgan JP.
      Spondylosis derformans in the dog. a morphologic study with some clinical and experimental observations.
      ,
      • Read RM
      • Smith RN.
      A comparison of spondylosis deformans in the English and Swedish cat and in the English dog.
      ,
      • Wright JA.
      A study of vertebral osteophyte formation in the canine spine. I. Spinal survey.
      ]. In animal studies, tensile overloading resulting in injuries to the Sharpey's fibers at the insertion of the annular ligament has been observed to result in endochondral ossification of the fibrocartilaginous repair tissue [
      • Jaffe H
      Metabolic, Degenerative and inflammatory diseases of the bone and joints.
      ,
      • G Schmorl HJ
      The human spine in health and disease.
      ]. Similarly, spondylophyte formation through enchondral ossification has been induced by repetitive extension loading [
      • Wada E
      • Ebara S
      • Saito S
      • Ono K.
      Experimental spondylosis in the rabbit spine: overuse could accelerate the spondylosis.
      ], by artificial ventral disc herniations [
      • Lipson SJ
      • Muir H.
      Vertebral osteophyte formation in experimental disc degeneration.
      ] and by injuries to the intervertebral disc [
      • Morgan JP.
      Spondylosis derformans in the dog. a morphologic study with some clinical and experimental observations.
      ]. These observations lead to the hypothesis, that spondylophytes could be the result of an accumulation of ossifying lesions.
      While spondylophytes have been measured to provide some protection against axial compression fractures [
      • Wagnac E
      • Aubin CÉ
      • Chaumoître K
      • Mac-Thiong JM
      • Ménard AL
      • Petit Y
      • et al.
      Substantial vertebral body osteophytes protect against severe vertebral fractures in compression.
      ], their biomechanical contribution during physiological axial compression has been observed to be rather small with values below 20% [
      • Al-Rawahi M
      • Luo J
      • Pollintine P
      • Dolan P
      • Adams MA.
      Mechanical function of vertebral body osteophytes, as revealed by experiments on cadaveric spines.
      ]. Similarly, the removal of ventral spondylophytes has been observed not to alter the trabecular strain in the vertebral bodies during axial compression [
      • Toh E
      • Yerby SA
      • Bay BK
      • McLain RF
      • Benson DR
      • Mochida J.
      The effect of anterior osteophytes and flexural position on thoracic trabecular strain.
      ], which indicate that spondylophytes do not provide much support as propping structure during physiological loading. The biomechanical role of spondylophytes in other loading situations remains largely unknown. The aim of this study is to quantify the biomechanical effect of spondylophytes during physiological loading in major loading conditions and to create a clinically meaningful classification system based on biomechanical data depending on the location and cranio-caudal extent of the spondylophytes.

      Materials and methods

      Preface

      Biomechanical data for the here presented analysis originate from a displacement controlled stepwise-reduction study conducted on 50 human spinal segments from T12- L5 (Science Care, Phoenix, AZ, USA). The overall study design and further details on the methodology are reported elsewhere [
      • Widmer J
      • Cornaz F
      • Scheibler G
      • Spirig JM
      • Snedeker JG
      • Farshad M.
      Biomechanical contribution of spinal structures to stability of the lumbar spine—novel biomechanical insights.
      ,
      • Cornaz F
      • Widmer J
      • Farshad-Amacker NA
      • Spirig JM
      • Snedeker JG
      • Farshad M.
      Biomechanical contributions of spinal structures with different degrees of disc degeneration.
      ] and are summarized in the following paragraphs. Ethical approval was obtained by the local authorities (BASEC Nr. 2017-00874). Before testing, computed tomography (CT) examinations (Somatom Edge Plus, Siemens Healthcare, Erlangen, Germany) were obtained and the specimens were carefully dissected from musculature and fat tissue without harming the bony structures, paraspinal ligaments and the intervertebral discs. An experienced radiologist identified and included all segments with spondylophytes (n=26) originating from 15 different donors (Table 1).
      Table 1Overview of all 26 specimens with spondylophytes
      LevelSexAge [y]Height [cm]Weight [kg]BMI
      number of spondylophytes.
      LocationMax. grade
      L1L2male861755016.21ventro-lateral3
      L3L4male861755016.21ventro-lateral2
      L1L2male65170122421ventro-lateral2
      L1L2male69188177502bilateral ventro-lateral2
      L3L4male69188177501lateral3
      T12L1male7017810031.61ventro-lateral4
      L2L3male7017810031.64combined3
      L4L5male7017810031.65combined4
      L2L3female7317011339.22bilateral ventro-lateral2
      T12L1male821788225.82bilateral ventro-lateral2
      T12L1male6618810028.21ventro-lateral2
      L2L3male6618810028.21ventro-lateral2
      L4L5male6618810028.22ventral and ventro-lateral4
      L2L3male661788627.31ventro-lateral2
      L4L5male661788627.32ventro-lateral and lateral1
      T12L1male751887922.35combined3
      L2L3male751887922.33combined2
      L1L2male821859126.44combined2
      L1L2male621737926.64combined3
      L3L4male621737926.62ventral and ventro-lateral2
      L2L3male751789028.42bilateral ventro-lateral1
      L4L5male751789028.41ventral2
      L2L3male751859828.42ventro-lateral and lateral2
      L4L5male751859828.41ventro-lateral1
      T12L1female5117310133.82bilateral ventro-lateral3
      L2L3male481788928.11ventro-lateral1
      70.218096.729.7
      low asterisk number of spondylophytes.

      Image analysis and spondylophyte grading

      A CT-based grading system for spondylophyte-classification was developed to quantify the cranio-caudal extent and categorize the location of spondylophytes (Fig. 1), inspired by the Brooker classification for heterotopic ossifications at the hip [
      • Brooker AF
      • Bowerman JW
      • Robinson RA
      • Riley LH.
      Ectopic ossification following total hip replacement. Incidence and a method of classification.
      ].
      Fig 1
      Fig. 1Spondylophyte classification is done by analyzing the cranio-caudal extent in relation to the disc space (grade 1–4) and by defining the location of the spondylophyte in relation to the vertebral body.

      Cranio-caudal extent

      The largest cranio-caudal extent of every spondylophyte was identified in the sagittal and coronal reformatted CT images and set in relation to the intervertebral disc space (Fig. 1). The classification system groups the spondylophytes in four grades: Grade 1 “minor spondylophytes”, grade 2 “moderate spondylophytes”, grade 3 “severe spondylophytes” and grade 4 “osseous bridging” (Fig. 2). Grade 1 is defined by the presence of spondylophytes spanning less than 50% of the disc-height, grade 2 by the combined extent of cranial and caudal spondylophyte being larger than 50%. Grade 3 is defined by the spondylophytes covering more than 90% of the disc-height or when a spondylophyte from one side of an endplate surpassed the height of the opposite endplate, grade 4 is defined by osseous bridging.
      Fig 2
      Fig. 2Computed tomography of samples illustrating the four grades of the cranio-caudal extent.

      Location

      The spondylophytes were categorized according to their anatomical location in relation to the vertebral body as “ventral”, “ventro-lateral”, “lateral”, “dorso-lateral” and “dorsal” with every sector covering 45° using axial CT images in correspondence to the sagittal or coronal reformatted images (Fig. 1). The position of the largest cranio-caudal extent defines the location of the spondylophyte.
      Two radiologists with >10 years of experience and specialized for musculoskeletal radiology assessed the CT-data of the spinal segments independently, closely following the classification algorithm.

      Biomechanical test setup

      The biomechanical experiments were performed at room temperature in a static testing machine with two integrated actuators (Zwick/Roell Allroundline 10kN and testXpert III Software, ZwickRoell GmbH & Co. KG, Germany). The system was complemented with a custom-made spine testing setup with different mounting positions allowing for the generation of flexion-extension (FE), lateral bending (LB) and axial rotation (AR) as well as axial compression-decompression (AC), anterior shear (AS), posterior shear (PS) and lateral shear (LS) loading (Fig. 3). The load was applied to the cranial vertebra with the caudal vertebra being fixed to the x-y-table, resulting in semi-constrained bending moments and translational forces. To allow for highly reproducible starting positions and load application, the setup was complemented with high precision bolts and fixtures for well-defined mounting of the individualized 3D-printed clamps [
      • Cornaz F
      • Fasser M-R
      • Spirig JM
      • Snedeker JG
      • Farshad M
      • Widmer J.
      3D printed clamps improve spine specimen fixation in biomechanical testing.
      ].
      Fig 3
      Fig. 3The setup for biomechanical testing used to test spinal segments. Figure adapted from
      [
      • Widmer J
      • Cornaz F
      • Scheibler G
      • Spirig JM
      • Snedeker JG
      • Farshad M.
      Biomechanical contribution of spinal structures to stability of the lumbar spine—novel biomechanical insights.
      ]
      .

      Biomechanical test protocol and data processing

      Biomechanical testing was based on a displacement-controlled stepwise-reduction approach. First, the intact spinal segments were loaded in FE, LS, LB, AS, AR and AC in a load-controlled fashion and the specific range of motion for each specimen was automatically registered and used for the following displacement-controlled test runs. The initial load-controlled test runs were performed with ±7.5 Nm in FE and LB with a velocity of 1 °/sec, ±7.5 Nm in AR with a velocity of 0.5 °/sec, ±150 N in AS/PS and LS with 0.5 mm/sec and +400 N/-150 N with 0.1 mm/sec in AC for the load-controlled tests. The same loading speeds were used for all consecutive displacement-controlled test runs. Recording was performed after five preloading cycles for each loading condition. The applied loading parameters conform to commonly used values in the literature representing physiological conditions [
      • Wilke HJ
      • Wenger K
      • Claes L.
      Testing criteria for spinal implants: recommendations for the standardization of in vitro stability testing of spinal implants.
      ]. Between the displacement-controlled tests, the transverse processes, the spinous processes, the facet joint capsule, the facet joints, the ligamentum flavum, the posterior longitudinal ligament, the anterior longitudinal ligament and finally the spondylophytes were resected. To limit unintentional injuries to the intervertebral disc and the vertebral bodies during spondylophyte resection, the CT scans were used to identify the exact location and extent of the spondylophytes. In most cases, resection was performed with a Luer forceps and a scalpel. In cases with larger spondylophytes, an oscillating saw was used to weaken the spondylophyte at its base before removal with the Luer forceps. The reduction in load required for the same motion was used to calculate the contribution of the resected structure. Further details on the method are published in previous studies [
      • Widmer J
      • Cornaz F
      • Scheibler G
      • Spirig JM
      • Snedeker JG
      • Farshad M.
      Biomechanical contribution of spinal structures to stability of the lumbar spine—novel biomechanical insights.
      ,
      • Cornaz F
      • Widmer J
      • Farshad-Amacker NA
      • Spirig JM
      • Snedeker JG
      • Farshad M.
      Biomechanical contributions of spinal structures with different degrees of disc degeneration.
      ].

      Statistical analyses

      The linear weighted agreement between the two readers (interobserver agreement) [
      • Landis JR
      • Koch GG.
      The measurement of observer agreement for categorical data.
      ] for the cranio-caudal extent of every spondylophyte was assessed. Based on classification system, the segments were categorized and grouped. In situations with more than one sample per group, the median values were reported. “Ipsilateral” movements were defined with the cranial vertebral body being loaded towards the spondylophyte, whereas “contralateral” indicates the opposite loading direction. Analogously, in configurations with more than one spondylophyte, the spondylophyte with the highest grade was used to define the direction “major”, while the opposite direction was defined as “minor”. Descriptive statistics were used to report the percentual contribution of the spondylophytes to the segmental stiffness in FE, AR, LB, LS, PS and AS. The recorded data during AC were not included into data analysis due to the movement amplitudes being too small for reproducible measurements with the here used test setup (about 0.2 mm movement for an amplitude of 1750 N).

      Results

      Out of the 50 spinal segments tested in the stepwise reduction study, 26 segments (52%) were affected by a total of 54 spondylophytes (Table 1). Isolated spondylophyte were present in 10 segments, a combination of two was observed in 10 segments and in six segments, more than two spondylophytes were present. 15 spondylophytes were categorized as grade 1, 22 spondylophytes as grade 2, 14 spondylophytes as grade 3 and 3 spondylophytes as grade 4.

      Interreader agreement

      In 74% (40 out of the 54 spondylophytes), the two readers agreed on the cranio-caudal extent. In the other 14 cases (26%), a difference of only one grade was present. Disagreement between grade 1 and 2 was present in 10 cases, between grade 2 and 3 in 3 cases and between grade 3 and 4 in one case. According to Landis and Koch [
      • Landis JR
      • Koch GG.
      The measurement of observer agreement for categorical data.
      ], interobserver agreement is “substantial” (linear weighted Cohen's kappa coefficient κ=0.73, p<.001). When combining minor and moderate spondylophytes (grade 1 and 2) to one group, interobserver agreement is “almost perfect” (linear weighted Cohen's kappa coefficient κ=0.86, p<.001) [
      • Landis JR
      • Koch GG.
      The measurement of observer agreement for categorical data.
      ].

      Biomechanical analysis

      The segments were grouped according to the grading system and the contribution to the segmental stiffness was reported for each group (Fig. 4): An isolated, ventral spondylophyte (grade 2) was recorded to contribute maximally in extension and only minimally in all other loading directions. Isolated lateral non-bridging spondylophytes (grade 1–3) contributed maximally during contralateral bending, while the contribution in all other loading directions was less than half. With an isolated ventro-lateral spondylophyte (grade 1–3), contralateral bending and extension were affected most prominently. In samples with combined spondylophytes at both ventro-lateral positions, lateral bending in both directions and extension were highly affected and the contribution in all other loading planes was again markedly smaller. In other combinations of multiple non-bridging spondylophytes, the results show larger variability but again, the contribution during contralateral bending in the presence of lateral spondylophytes and during extension in the presence of a ventral osteophyte were affected most severely. With osseous bridging (grade 4), all loading planes were affected with values ranging from 25% to 86%. The data of one specimen was not included due to complete ossification of the intervertebral disc.
      Fig 4
      Fig. 4A: Percentage of spondylophyte contribution (median) in flexion, extension, lateral bending, axial rotation, lateral shear, anterior shear and posterior shear (red) classified according to spondylophyte location and grade. n=number of specimens per group. B (continued): Percentual spondylophyte contribution (median) in flexion, extension, lateral bending, axial rotation, lateral shear, anterior shear and posterior shear (red) classified according to spondylophyte location and grade. n=number of specimens per group.
      Fig 4
      Fig. 4A: Percentage of spondylophyte contribution (median) in flexion, extension, lateral bending, axial rotation, lateral shear, anterior shear and posterior shear (red) classified according to spondylophyte location and grade. n=number of specimens per group. B (continued): Percentual spondylophyte contribution (median) in flexion, extension, lateral bending, axial rotation, lateral shear, anterior shear and posterior shear (red) classified according to spondylophyte location and grade. n=number of specimens per group.

      Discussion

      As the role of spondylophytes on segmental stiffness is largely unknown, we aimed at quantifying the biomechanical effect of spondylophytes depending on their location and their cranio-caudal extent in major loading planes. A clinically applicable classification system with substantial interobserver agreement is presented in order to facilitate further research and to provide a clinically applicable tool for the assessment of spondylophytes.
      The biomechanical effectiveness of spondylophytes is depending on their location and cranio-caudal extent. For isolated, non-bridging spondylophytes (grade 1-3), the most prominent effect on segmental stiffness is observed during contralateral bending (e.g., bending to the right-hand side for left lateral spondylophytes and extension for ventral spondylophytes). Ipsilateral bending (towards the spondylophyte), translational loading, as well as the other tested loading directions are affected to a lesser degree. While larger spondylophytes tend to be more effective than smaller ones, even severe spondylophytes (grade 3) provide less than 35% to the segmental stiffness during contralateral bending and below 13% in all other loading directions. These results indicate that even large isolated non-bridging spondylophytes (grade 1–3) do not provide much additional stiffness to a spinal segment. In situation with more than one spondylophyte, the results are more variable, however contralateral bending in relation to the spondylophyte location is still affected most prominently. In specimens with bony bridging (grade 4), the contribution to the segmental stiffness reaches values of over 80%. In these cases, the spinal segment can be regarded as functionally fused and the bony bridge is responsible for a large portion of the segmental stiffness.
      Non-bridging spondylophytes are relatively ineffective during ipsilateral bending, where the spondylophytes would act as propping structures. This small effectiveness as a propping structure is supported by the limited literature on this topic [
      • Wagnac E
      • Aubin CÉ
      • Chaumoître K
      • Mac-Thiong JM
      • Ménard AL
      • Petit Y
      • et al.
      Substantial vertebral body osteophytes protect against severe vertebral fractures in compression.
      ,
      • Al-Rawahi M
      • Luo J
      • Pollintine P
      • Dolan P
      • Adams MA.
      Mechanical function of vertebral body osteophytes, as revealed by experiments on cadaveric spines.
      ,
      • Toh E
      • Yerby SA
      • Bay BK
      • McLain RF
      • Benson DR
      • Mochida J.
      The effect of anterior osteophytes and flexural position on thoracic trabecular strain.
      ]. This biomechanical behavior is contra intuitive due to the claw-like shape of most spondylophytes, which suggest a propping role. However, this behavior can be explained by the characteristics of the tissue spanning the gap between non-bridging spondylophytes, which is mainly composed by annulus fibrosus fibers and parts of the anterior longitudinal ligament [
      • Pate D
      • Goobar J
      • Resnick D
      • Haghighi P
      • Sartoris DJ
      • Pathria MN.
      Traction osteophytes of the lumbar spine: radiographic-pathologic correlation.
      ]. We hypothesize, that this tissue acts primarily as a ligamentous structure resulting in relevant resistance against tensile loading but limited resistance to compressive stresses. In situations with larger spondylophytes, the span witdh is reduced and the tissue is less extendible explaining for the grade-dependent contribution pattern.
      The finding that non-bridging spondylophytes (grade 1–3) are relatively ineffective as a propping structure and do not provide relevant stiffness to the spinal segment has important clinical implications. Many surgeons will choose not to include an intervertebral cage during spinal fusion in the presence of large anterior spondylophytes, due to the theory of spondylophytes acting as a propping structure and thus providing sufficient stiffness in flexion. However, based on the here presented biomechanical data, this concept is questionable: Large, non-bridging anterior spondylophytes primarily increase stiffness in extension rather than flexion. In conclusion, these spondylophytes do not appear to be able to compensate for the anterior propping support of an intervertebral cage. Only in cases with bridging spondylophytes (grade 4), the spinal segment can be regarded as functionally fused and implantation of an intervertebral cage can potentially be omitted from a biomechanical perspective. While this biomechanical consideration provides another element in the decision process of whether an intervertebral cage should be included in a posterior spinal fusion construct, it does not omit the necessity to consider all other factors such as symptoms and clinical presentation, the need for deformity or spinal alignment correction, bone quality or the risk for non-union.
      Spondylophytes are located more frequently at the concavity of scoliotic curves [
      • Nathan H.
      Osteophytes of the vertebral column.
      ]. The here presented data provides an explanation for the correlation between spondylophytes and curve rigidity [
      • Zhu F
      • Bao H
      • Yan P
      • Liu S
      • Bao M
      • Zhu Z
      • et al.
      Do the disc degeneration and osteophyte contribute to the curve rigidity of degenerative scoliosis?.
      ] and the association between unilateral spondylophytes and curve progression [
      • Jimbo S
      • Kobayashi T
      • Aono K
      • Atsuta Y
      • Matsuno T.
      Epidemiology of degenerative lumbar scoliosis: a community-based cohort study.
      ] in patients suffering from degenerative scoliosis. The effect of spondylophyte-resection on the segmental range of motion could not be analyzed with the data of this study due to the displacement-controlled test protocol. However, this effect should be further investigated as the potential benefit of reestablishing a more physiological motion pattern with spondylophyte resection could be very helpful in the clinical practice, such as in the surgical treatment of scoliotic spines. Furthermore, with the scarcity of non-degenerated cadaveric specimens for biomechanical testing, changing segmental motion patterns to a more physiological state could be very valuable.
      -The here presented study is associated with some limitations: Due to the large number of subgroups in the classification system, statistical analysis of the data was not possible and only qualitative evaluation was performed. Spondylophyte-resection without harming annulus fibrosus fibers is not always possible, resulting in a possible overestimation of the contribution of the spondylophytes to spinal stiffness, especially in loading configuration resulting in tensile loading of the annulus fibrosus fibers. Further, in the present study, isolated moments and forces are applied, which is a gross simplification of the complex loading conditions in-vivo. However, this simplification allows for welldefined, reproducible loading parameters, which are crucial for such a study. To generate pure moments and pure translational forces, the translational plane had to be unconstrained. This could allow for small differences in translational movements after spondylophyte-resection, resulting in a slight over- or underestimation of the biomechanical contribution. Nevertheless, the results are robust enough to allow conclusion of the main findings of the study, namely the relation between the location and cranio-caudal extent of spondylophyte with their biomechanical effectiveness and the major contribution of spondylophytes being during contralateral bending. These biomechanical observations, not yet reported in the literature, allowed to create a simple classification system with substantial interobserver agreement. Certainly, further research is needed to apply the classification system to specific clinical questions.
      In conclusion, the location and cranio-caudal extent of spondylophytes are essential parameters influencing the biomechanical effect on segmental stiffness. A reproducible classification was biomechanically validated and is presented. With this, the effect of specific spondylophyte configurations on segmental stiffness become more predictable and supports surgical decision making.

      Acknowledgments

      Imaging was performed with support of the Swiss Center for Musculoskeletal Imaging, SCMI, Balgrist Campus AG, Zürich, with special acknowledgement to Natalie Hinterholzer and Daniel Nanz.

      Declarations of Competing Interests

      The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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