Received 28 May 2004; accepted 5 October 2005

0268-0033/$ - see front matter Published by Elsevier Ltd.

doi:10.1016/j.clinbiomech.2005.10.001

An exploratory study of loading and morphometric factors
 

associated with specific failure modes in fatigue testing
 

of lumbar motion segments
 

Sean Gallagher a,*,

a National Institute for Occupational Safety and Health, Mining Injury Prevention Branch, P.O. Box 18070, Pittsburgh, PA 152360070, USA
 

William S. Marras b,

b Biodynamics Laboratory, The Ohio State University, Columbus, OH 43210, USA
 

Alan S. Litsky c,

c Orthopaedic BioMaterials Laboratory, The Ohio State University, Columbus, OH 43210, USA
 

Deborah Burr d

d Department of Health Services, Research Management, and Policy, University of Florida, Gainesville, FL 32611, USA
 

Abstract

Background. There is currently little information regarding factors associated with specific modes of motion segment failure using

a fatigue failure model.

Methods. Thirty-six human lumbar motion segments were fatigue tested using spinal compressive and shear loads that simulated lifting a 9 kg weight in three torso flexion angles (0°, 22.5°, and 45°). Twenty-five segments failed via fatigue prior to the

10,000 cycle maximum. These specimens were visually inspected and dissected so that the mode(s) of failure could be determined.

Failure modes included endplate fractures (classified into nine varieties), vertebral body fractures, and/or zygapophysial joint disruption. Logistic regression analyses were performed to determine whether certain morphometric variables, amount of motion

segment flexion, disk degeneration scores, and/or loading characteristics were associated with the occurrence of specific failure

modes.

Findings. Results indicated that stellate endplate fractures were associated with increased posterior shear forces (P < 0.05) and

less degenerated discs (P < 0.01). Fractures running laterally across the endplate were associated with motion segments having larger

volumes (P < 0.01). Endplate depression was more common in smaller specimens (P < 0.01), as well as those experiencing increased

posterior shear force (P < 0.05). Zygapophysial joint damage was more likely to occur in a neutral posture (P < 0.01).

Interpretation. These results suggest that prediction of failure modes (e.g., specific endplate fracture patterns) may be possible (at

least for older specimens) given knowledge of the spinal loads along with certain characteristics of the lumbar spine.

Published by Elsevier Ltd.

1. Introduction

As with any material, spinal tissues will fail when an

applied load exceeds the tissue tolerance (Litsky and

Spector, 1999). Failure may be the result of a single

application of a large load (exceeding the ultimate

strength of the material) or may result from repeated

application of a sub-maximal load via fatigue failure

(McGill, 1996). Given the repetitive nature of spine

loading in many occupational (as well as non-occupational) settings (Brinckmann et al., 1988; Marras

et al., 1993), the latter scenario would seem orthopaedically significant. Nonetheless, fatigue failure of lumbar

tissues has received relatively little attention in the

literature.
S. Gallagher et al. / Clinical Biomechanics 21 (2006) 228–234 229

The magnitude and distribution of loads on structural components of the lumbar spine vary considerably based upon numerous factors, and these will

influence the structures and/or patterns of failure

observed. Among the factors influencing load magnitude and distribution are the posture adopted by a

motion segment (White and Panjabi, 1978), the amount

and distribution of bone mineral content (Hayes, 1986;

Rockoff et al., 1969), the size of the vertebral bodies

and discs (Jager and Luttmann, 1991; White and Panjabi, 1978), the degree of disc degeneration (Kulak

et al., 1976), and the magnitude of the compressive

and shear forces imposed upon the spine (Jager and

Luttmann, 1991; Begemann et al., 1994). As an example, zygapophysial joints are thought to bear approximately 15–20% of the compressive load experienced

by a motion segment in a neutral position (Adams

and Hutton, 1980; Adams and Hutton, 1983). However, when the spine is flexed, this loading path may

be reduced (White and Panjabi, 1978) and the compressive load may be increasingly borne by the inter-body

joint (the joint comprised of two vertebral bodies and

their adjoining disk). The increased burden experienced

by the inter-body joint would amplify the stress

imposed on the vertebral endplates and discs, which

will experience additional strain and increased potential

for failure.

The vertebral endplate appears to be the tissue most

likely to experience initial failure in tests of both ultimate compressive strength and fatigue failure (Brown

et al., 1957; Perey, 1957). A variety of endplate fracture patterns have been observed and Brinckmann

et al. (1988) developed a useful classification system

for various modes of endplate damage. Vertebral body

fractures and disruption of the zygapophysial joints are

also observed in compressive loading tests; however,

failure of the intervertebral discs are less frequent

(Bogduk, 1997). Discs may fail when compressed in

flexion (Adams and Hutton, 1982) when compressed

in flexion combined with an axial twist (Gordon

et al., 1991), or as the result of a cascade initiated by

endplate failure (Adams et al., 2000). Research using

porcine models has suggested that disc herniation also

can be caused by repeated flexion and extension under

moderate compressive loads (Callaghan and McGill,

2001).

Evaluating factors associated with specific failure

modes exhibited by lumbar motion segments may assist

in developing improved models of the manner of tissue

failure and may ultimately assist in our understanding

of the etiology of low back pain. Accordingly, the current exploratory study was performed to determine factors associated with specific failure modes in a study

examining fatigue failure of lumbar motion segments

exposed to loadings estimated to occur when lifting in

various torso flexion postures.

2. Methods

Twelve fresh, frozen lumbar spines, with a mean age

of 81 years (SD 8) were obtained from the Anatomical

Gift Program at Wright State University. Specimens

were excised within 24 h after death from subjects having no history of spinal disease or prolonged bed rest

prior to death. Specimens were thawed at room temperature prior to dissection and testing. Intact lumbar

spines were dissected into three separate motion segments: L1–L2, L3–L4, and L5–S1.

Anterior–posterior (A–P) and left lateral (LLAT)

radiographs of each intact motion segment were

obtained and served to detect the presence of existing

defects in individual motion segments and were used

to make various morphometric measurements of intact

motion segments via measurement tools provided in

eFilm xray viewing software (Merge eFilm, Milwaukee,

WI, USA). Estimates of the volume of the inter-body

joint (i.e., two vertebral bodies and intervening disc,

not including posterior elements) of each motion segment were calculated on the basis of selected dimensions

of the vertebral bodies and discs.

Vertebral bodies were potted in trays containing

polymethylmethacrylate (PMMA), the orientation to

the vertical of each motion segment being confirmed

by endplate measurements obtained via multiple radiographs during the fixation process. Once specimens were

properly oriented according to the torso flexion posture

being simulated, they were placed in test fixtures

attached to a servohydraulic test frame [Bionix 858,

MTS Systems, Eden Prairie, MN, USA]. The test fixtures were situated within an environmental chamber

whose temperature was kept at approximately 37 °C.

Moisture was introduced into the chamber to maintain

a humid environment.

Care was exercised to reproduce compressive and

shear loads and spinal postures adopted when lifting a

9 kg box in three trunk flexion angles: 0° (neutral posture, as if standing erect), 22.5° (partial flexion), and

45° (full flexion). A dynamic electromyographicallyassisted biomechanical model was used to develop

appropriate compressive and shear loads and rates of

loading at each torso flexion angle and lumbar level

(Granata and Marras, 1995; Marras and Granata,

1997; Marras et al., 2001; Jorgensen et al., 2001). Details

of the loadings used can be obtained in Table 1. Motion

segments within each spine were randomly assigned to

torso flexion angles. Motion segments were creep loaded

for 15 min and then cyclically loaded (using load control) at 0.33 Hz until failure or the maximum number

of cycles (10,000) was completed. Failure was defined

as a displacement of 10 mm after termination of the period of creep loading. Twenty-five of the 36 motion segments failed via fatigue before the maximum number of

cycles were completed. Those that lasted were subjected
230 S. Gallagher et al. / Clinical Biomechanics 21 (2006) 228–234

to a test of ultimate compressive strength. The latter were

not included in the present analysis due to the extensive

damage associated with this mode of testing.

Upon completion of the mechanical testing, specimens were removed from the loading jigs and taken to

the radiology clinic to evaluate damage using a lateral

radiograph. These radiographs were read to evaluate

the post-test status of the endplates, vertebral bodies,

trabeculae, intervertebral discs, and posterior elements.

Visual inspection of failed specimens was performed to

evaluate external evidence of failure, particularly facet

disruption and/or external evidence of fracture to the

vertebral bodies. The PMMA-specimen interface was

scrutinized to ensure that failure did not occur at this

interface. Failed specimens were dissected through the

mid-plane of the intervertebral disc, digitally photographed and a Galante disc degeneration score assigned

to each of the discs. The endplates were then exposed

and assessed for damage.

The Brinckmann et al. (1988) classification scheme

did not fully characterize the nature of the endplate

fractures observed in this investigation, and a modified

version of the classification system was developed. This

new classification system, illustrated in Fig. 1, includes

many of the original Brinckmann et al. (1988) classifications, but adds some additional classifications of endplate damage (ring fractures, lateral fractures and A–P

fractures) observed in the current study. Two of the

Brinckmann et al. (1988) classifications were omitted

in this new system. These included the ‘‘transverse’’

fracture, which appears to represent a fracture of the

vertebral body rather than the endplate, and the ‘‘Y’’

fracture, observed only twice in the Brinckmann et al.

(1988) original experiment, and not observed in the

present study.

Table 1

Endplate fracture patterns and zygapophysial joint damage experience for motion segments failing via fatigue in simulated lifting of 9 kg load in

different torso flexion angles

Spine

ID

Motion

segment

Torso

flexion

Absolute

motion

segment

flexion

Motion

segment

flexion

Compression

(N)

Shear

(N)

Load

rate

(N/s)

Disk

grade

Inferior

EP (Sup.

Vertebra)

Superior EP

(Inf. Vertebra)

Zygapophysial

joint damage

M11 L1–L2

L3–L4

22.5

45

1

-2

1

6

2157

2700

-1052

-1622

2100

4800

3

3

1,6 4

9

*

M8 L1–L2 45 3 3 2878 -1281 4800 2 6 6

M1 L1–L2

L3–L4

L5–S1

0

22.5

45

0

-5

-14

0

3

6

1178

2255

3127

-549

-821

-541

700

2100

4800

3

2

2

2

2,1

2,6

*

*

F9 L1–L2

L5–S1

45

0

3

-20

3

0

2878

1196

-1281

507

4800

700

3

3

4,5 5

6 *

M7 L1–L2

L5–S1

22.5

45

1

-14

1

6

2157

3127

-1052

-541

2100

4800

3

4

6,5

6

6

*

F6

F17

L3–L4

L1–L2

L3–L4

L5–S1

45

22.5

45

0

-2

1

-2

-20

6

1

6

0

2700

2157

2700

1196

-1622

-1052

-1622

507

4800

2100

4800

700

2

3

2

2

1

1

6

6

1,6

6

*

*

*

M10 L1–L2

L5–S1

45

22.5

3

-17

3

3

2878

2386

-1281

251

4800

2100

2

3

1,4 8

4,5,6 *

F13 L1–L2

L1–L4

L5–S1

0

22.5

45

0

-5

-14

0

3

6

1178

2255

3127

-549

-821

-541

700

2100

4800

3

2

2

6

1,6

1

6

1

*

M16 L1–L2

L3–L4

45

22.5

3

-5

3

3

2878

2255

-1281

-821

4800

2100

2

1

1

1,5 *

M12 L1–L2

L5–S1

22.5

45

1

-14

1

6

2157

3127

-1052

-541

2100

4800

3

3

2,7

2,5

M14 L3–L4

L5–S1

45

22.5

-2

-17

6

3

2255

2386

-821

251

4800

2100

2

3

1

6,5

6,5

6,5

Disc degeneration grades are given per Galante (1967). Refer to Fig. 1 for classification of endplate fractures.

2.1. Data analysis

A series of stepwise logistic regression analyses were

performed to evaluate the association between various

motion segment and load characteristics and failure

modes observed in post-test examination and dissection.
S. Gallagher et al. / Clinical Biomechanics 21 (2006) 228–234 231

Fig. 1. Endplate fracture classification scheme modified from Brinckmann et al. (1988).

The analysis was performed on the 25 motion segments

failing via fatigue failure; thus, results represent a conditional probability based on failure by this mode.

Independent variables included motion segment characteristics including Galante disc degeneration grade

(Galante, 1967), estimated volume of the inter-body

joint, the degree of flexion from a neutral position,

and weight (g) of the motion segment. Loading characteristics, comprising the balance of independent variables, included compressive and shear forces

experienced by the motion segment and the rate at

which specimens were loaded. Each failure mode (the

nine endplate fracture patterns, fractures of superior

and inferior vertebral bodies, and zygapophysial joint

disruption) was treated as the dependent variable in separate stepwise logistic regressions using the independent

variables listed above. As an exploratory analysis,

multiplicity corrections were not applied in the data

analyses (Bender and Lange, 2001). Specifically, a comparisonwise Type I error rate alpha level of 0.05 was

employed.

3. Results

Table 1 provides a summary of motion segment characteristics along with endplate fractures patterns and

occurrence of zygapophysial joint damage observed for

all motion segments failing via fatigue in the experiment.

Table 2 provides results of the logistic regression analyses relating specific failure modalities to the various

independent factors manipulated in the study.

3.1. Endplate fracture patterns

Several endplate fracture patterns were associated

with specific changes in the independent variables under

study (Table 2). Stellate endplate fractures were associated with less degenerated discs (P < 0.005) and

increased shear forces on the motion segment (P <

0.05). Fissures running laterally across the endplate were

observed to occur more frequently with motion segments of larger volume (P < 0.005). Depression of the

endplate was a more frequent finding in specimens having smaller volume (P < 0.01) and experiencing higher

levels of shear force (P < 0.05).

3.2. Zygapophysial joints

As can be seen in Table 2, zygapophysial joint damage was significantly associated with the degree of torso

flexion (P < 0.01). Examination of Table 1 shows that

zygapophysial damage was present in 100% of the specimens failing via fatigue in the simulated neutral trunk

posture. Damage was observed in three of nine (33%)

specimens in the 22.5° torso flexion condition, and three

out of twelve specimens (25%) exposed to the 45° torso

flexion condition exhibited damage. Thus, the likelihood

of damage to the facets was greatest in the neutral posture, and was diminished as greater flexion of the

motion segment was assumed.

4. Discussion

This investigation is the first, to the authors' knowledge, to uncover statistical associations between both

Table 2
 

Summary of significant logistic regression results relating variables to specific failure modes (Note: MS = motion segment, AP = anterior–posterior,
 

EP = endplate)
 

Failure mode Significant variable associations P Nature of association

Stellate EP fracture Galante grade

AP shear

0.006

0.019

#Galante: "Stellate fracture

"Post. Shear: "Stellate fracture

Lateral EP fracture MS volume 0.003 "Volume: "Lateral fracture

EP depression MS volume

AP shear

0.006

0.015

#Volume: "EP depression

"Post. Shear: "EP depression

Facet damage Torso flexion 0.009 #Flexion: "Facet damage
232 S. Gallagher et al. / Clinical Biomechanics 21 (2006) 228–234

motion segment loading characteristics and the occurrence of specific endplate fracture patterns and zygapophysial joint damage. Factors found to influence

endplate fracture patterns include the degree of disc

degeneration of the specimen, the size of the specimen,

and the amount of shear force experienced. Zygapophysial joint damage was influenced by the posture adopted

by motion segments failing via fatigue.

Several of the associations uncovered in this investigation appear readily interpretable. For example, stellate endplate fractures were found to be associated

with greater shear force exposure and less degenerated

discs. Bone is an anisotropic material and is more susceptible to damage when exposed to shear force (Litsky

and Spector, 1999). It may be that exposure to higher

shear forces undermines the support of the endplate

via damage to the underlying trabecular arcades. The

more centralized pressure distribution on the endplate

associated with less degenerated discs (Bogduk, 1997),

combined with the reduced support of the endplate

resulting from trabecular shear damage, and may result

in a stellate fracture pattern where a focal area of fracturing is observed centrally in the endplate with cracks

radiating to the periphery.

Motion segments having smaller volumes and higher

shear forces were associated with increased incidence of

endplate depression. It should be pointed out that the

compressive and shear loads were identical no matter

the size of the specimen. Thus, smaller specimens would

experience a more concentrated distribution of stress

that may increase the likelihood of endplate depression.

Larger specimens would have the same force distributed

over a larger area, which may decrease the propensity to

centrally depress the endplate. Increased shear force

may again undermine the support of the endplate leading to increased incidence of depressed endplates.

This study involved the modification of an endplate

fracture classification structure proposed by Brinckmann et al. (1988). Results clearly support the use of

an endplate damage classification system, as different

endplate damage classifications were observed to have

significant associations with certain motion segment

and loading characteristics. Two of the original Brinckmann et al. (1988) classifications were found to have significant associations with such characteristics (i.e.,

stellate fractures and endplate depressions). However,

one of the new endplate fracture classifications (a fracture running laterally across the endplate) was also

found to exhibit a significant association with specimen

morphometry. This result would seem to support the

suggested modifications of the original classification system. As research in this area continues, it may be possible to develop further refinements to endplate damage

classifications. Such a process may continue to improve

our understanding of the factors associated with the

manner of endplate failure.

Studies have indicated that compression of a motion

segment in a neutral posture may lead to damage to the

zygapophysial joints, a finding supported by the current

analysis. When subject to severe or repeated compression in this position, the superior facets impact the lamina below, pushing the facets backwards, ultimately

resulting in joint disruption. In a flexed position, these

joints assume a progressively smaller load-bearing

responsibility (White and Panjabi, 1978) and failure

appears to occur primarily in the inter-body joint with

a progressively lower likelihood of facet involvement.

It is remarkable that, even given a relatively small

sample of motion segments, several significant associations were uncovered relating morphologic and loading

variables to specific failure patterns. Results suggest that

by knowing certain characteristics of the spine and the

manner of loading, one may be able to predict which

structures may be at increased risk of failure and perhaps even predict what pattern of that failure might

result. It is noteworthy that most of the significant independent variables used in this analysis (degree of disc

degeneration, size of the specimen, shear forces) can be

measured or estimated using in vivo techniques. The

current results certainly suggest the possibility that such

measures could be evaluated in vivo and may allow prediction as to the likely structure of failure in the lumbar

spine and even the likely failure pattern. However, one

should bear in mind that the results of the current study

are exploratory in nature and will need to be tested in

further confirmatory studies. Clearly, much additional

research will be necessary to confirm the present results

and potentially identify additional associations.

A complete assessment of the experimental results

described above requires the consideration of certain

limitations. The first of these deals with the age of the

cadaveric cohort studied. Unfortunately, the vendor

used to obtain the lumbar spines used in this study

was unable to provide specimens under the age of 65.

As a result, it becomes difficult to generalize the results

of this study to the younger, working age population

that is the intended beneficiary of the research. Younger

spines would be expected to have increased bone mineral

content and density than the older spines tested in this

study, and failure patterns may differ as a result. Efforts

are currently underway to obtain a sample of spines

more representative of a working age population to continue this research. It may be noted that specimens were

loaded in compression and shear with motion segments

preset at the desired Cobb angles, instead of generating

the motion segment flexion via an anterior offset in the

application of force. Analysis of free body diagrams

demonstrate that whether the motion segment is preset

in flexion or flexed to the same degree by applying a

bending moment, application of equivalent compressive

and shear forces will result in equivalent reaction forces

being experienced by the specimen. The current loading
S. Gallagher et al. / Clinical Biomechanics 21 (2006) 228–234 233

situation did not generate a ‘‘rocking’’ motion of the

motion segment as an offset load would; however, the

authors opted for the more precise control offered by

loading the specimen at the desired flexion angle.

The lumbar spine is one part of a complex physiologic system and isolation of the spine (or its motion segments) necessarily alters the loading situation compared

to the in vivo environment. Studies performed on animals have suggested a possible change in mechanical

behavior of various tissues after death (Keller et al.,

1990); however, the differences attributed to death in

this experiment were not much larger than trial to trial

variability on the live animal (Adams and Dolan,

1995). However, the process of dissecting out motion

segments necessitates a weakening of ligaments of the

spine that have fibers spanning multiple vertebrae

(Adams, 1995). There are also obvious differences

between the manner in which spine segments are loaded

with functioning muscles and tendon attachments as

opposed to a specimen potted in polymethylmethacrylate and loaded in a test frame. Nonetheless, the methods

of in vitro testing employed here remain one of our best

methods to improve our understanding of the mechanical responses of lumbar tissue.

While radiographs were obtained and abnormal

external findings were noted during dissection, it is possible that pre-existing damage, particularly to the endplates, may have been present prior to testing but not

detected. It is extremely difficult to detect endplate

fractures via regular radiographs or other imaging

techniques (White and Panjabi, 1978). Thus, it is conceivable that some of the damage reported in the posttest evaluations was pre-existing, and not the result of

the stresses imposed during testing. Certainly the tests

could have also exacerbated pre-existing damage in the

specimens, causing failure to occur more quickly than

would have occurred to an intact specimen. However,

the statistical results obtained in this analysis indicate

that the associations uncovered are beyond random

chance occurrences. Thus, unless we believe that the randomization procedure was extremely unlucky, we must

conclude that the failure modes observed are influenced

by the factors identified above.

5. Conclusions

On the basis of the current investigation, the following conclusions are drawn:

1. Endplate fractures patterns and zygapophysial joint

damage in this older cohort of lumbar spines were

significantly associated with variables such as motion

segment morphometry, degree of flexion, disk degeneration, and the nature of the applied loads in fatigue

failure.

2. Stellate	 endplate fractures were associated with

increased shear exposure and less degenerated disks.

Lateral endplate fractures were found to be associated with specimens with larger inter-body joint volume. Endplate depression was associated with lower

exposure to shear and smaller specimens.

3. Zygapophysial joint damage was more likely in the

neutral posture condition, and progressively less

likely with increasing flexion in specimens failing via

fatigue.

4. A modified endplate damage classification system is

suggested, and data from this study provide support

for the modified system.

5. Results	 suggest that prediction of specific failure

modes for older lumbar motion segments may be possible given knowledge of the specimen size, disk

degeneration status, degree of flexion and spine loading characteristics.

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