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SPINE Volume 28, Number 19, pp 2204–2208

©2003, Lippincott Williams & Wilkins, Inc.

Failure of Human Cervical Endplates: A Cadaveric


Experimental Model

Eeric Truumees, MD,* Constantine K. Demetropoulos, PhD,† King H. Yang, PhD,‡ and
Harry N. Herkowitz, MD‡

Study Design. An in vitro biomechanical study using a graft, anterior interbody fusion, endplate, bone density,
servohydraulic testing machine on cadaveric endplates. compressive strength, postoperative complications]
Objectives. To characterize the effects of bone mineral Spine 2003;28:2204 –2208
density, endplate geometry, and preparation technique
on endplate failure load.
Summary of Background Data. The effects of endplate
preparation methods on failure loads are only partly char- Anterior cervical discectomy and corpectomy techniques
acterized in the literature. Endplate burring has been recom- are commonly employed in the treatment of radiculopa-
mended to increase fusion rates. However, graft subsidence thy and myelopathy. Occasionally, these procedures are
may complicate anterior reconstruction procedures. complicated by graft collapse or extrusion, endplate fail-
Methods. After radiographic screening, 21 cadaveric
cervical spines underwent dual-energy x-ray absorptiom-
ure and subsidence, or nonunion.1 Presently, the optimal
etry scanning to quantify mineral content. Endplate ge- compressive force to decrease bone graft extrusion and
ometry was calculated in 55 randomly selected endplates encourage fusion is not known.2,3,4,5
from the inferior C2 to the superior T1 levels. These ver- The ability of various grafts to withstand compressive
tebrae were embedded in polyester resin and randomly loading has been characterized. White and Hirsh tested
left intact, perforated, or burred. The cervical endplates
were loaded at a rate of 0.2 mm/s on an Instron materials
various grafts employed in anterior cervical spine sur-
tester with an attached 9 mm diameter polycarbonate rod gery. 6 They found that Smith-Robinson tricortical
(an area of 64 mm2). A stepwise, univariate linear regres- wedges were significantly stronger (344 kp) than other
sion was used to compare the point of endplate failure graft configurations (188 –195 kp). The authors esti-
with the vertebral level, endplate area, gender, age, bone mated that these grafts would be subjected to 6.3 kg of
mineral density, and preparation technique.
Results. Mean bone mineral density, as measured by
force. They did not include postoperative compressive
dual-energy x-ray absorptiometry, was 0.713 g/cm2 (⫾ forces from muscle tension or neck flexion.
0.173 g/cm2). Mean endplate area was calculated at 323 Wittenberg et al studied compressive strengths of var-
mm2. A mean compressive force of 754 N (⫾ 445 N) was ious grafts under axial compression.7 In this study, fibu-
required before endplate failure. Trends toward increas- lar strut grafts withstood 5070 N (⫾ 3.250 N) of axial
ing compressive loads were noted with decreasing end-
plate area and increasing bone mineral density. Increas-
loading before failure. Failure was defined as the maxi-
ing age (P ⫽ 0.0203), caudal vertebral level (P ⬍ 0.0001), mum load on the load-displacement curve. Fibular strut
endplate burring (P ⫽ 0.0068), and female gender (P ⫽ grafts were significantly stronger than anterior (1150 ⫾
0.0452) were associated with significantly lower endplate 487 N) and posterior (667 ⫾ 311 N) iliac crest and rib
fracture loads in compression. (452 ⫾ 192 N) grafts.
Conclusions. Bone quality was predictive of endplate
compressive failure loads. Intact endplates failed at sig-
An et al used six fresh frozen cadaveric pelves to assess
nificantly higher loads than their perforated or burred the potential usefulness of dual-energy x-ray absorpti-
counterparts. [Key words: cervical spine, biomechanics, ometry (DEXA) to predict the strength of iliac crest bone
grafts.8 They reported that the biomechanical strength of
iliac bone is linearly related to its bone mineral density
(BMD) as measured by DEXA. Their Smith-Robinson
From the †Department of Orthopaedic Surgery, *William Beaumont grafts failed at 1368 N. Anterior iliac crest strut grafts
Hospital, Royal Oak, and ‡Bioengineering Center, Wayne State Uni- failed at 2168 N.
versity, Detroit, Michigan. Endplate failure loads have not been as well charac-
This study was funded, in part, by an unrestricted grant from
Medtronic-Sofamor-Danek. terized. In one study of an entire motion segment, the
This paper was presented, in part, at the 28th Annual Meeting of the cervical vertebral body could withstand compressive
Cervical Spine Research Society; 2000; Charleston, South Carolina. loads of 1310 N.4 Lim et al studied endplate preparation
Acknowledgment date: April 15, 2002. First revision date: June 28,
2002. Second revision date: September 18, 2002. Acceptance date: techniques and found that intact endplates failed at a
January 24, 2003. mean compressive load of 634 N.9 Partly burred end-
The manuscript submitted does not contain information about medical plates failed at 494 N, whereas completely burred end-
device(s)/drug(s).
Corporate/Industry funds were received to support this work. No ben- plates failed at 419 N. These authors used a finite ele-
efits in any form have been or will be received from a commercial party ment model to assess the effects of endplate perforation
related directly or indirectly to the subject of this manuscript. on endplate failure loads. The effect of one large central
Address correspondence to Christine Musich, 3535 West 13 Mile
Road, Suite 605, Royal Oak, MI 48073, USA; E-mail: hole was compared to two- and four-hole configura-
Truumees@Comcast.net tions. They found that one large central hole was prefer-

2204
Cervical Endplate Compression Load • Truumees et al 2205

Table 1. Distribution of Cervical Spine Specimens


Sample Area Failure BMD Age
Preparation Size (mm2) Load (N) (g/cm2) (yrs)

Intact 35 314 ⫾ 106 897 ⫾ 453 0.723 ⫾ 198 72 ⫾ 13


Perforated 10 348 ⫾ 111 590 ⫾ 347 0.681 ⫾ 108 74 ⫾ 16
Burred 10 326 ⫾ 101 403 ⫾ 208 0.676 ⫾ 119 70 ⫾ 16
BMD ⫽ bone mineral density.

able in that it better distributed compressive load across


the remaining intact endplate.
We postulate that three variables affect load to failure
of cervical endplates in anterior fusion procedures: end-
plate geometry, bone quality, and endplate preparation
technique. Endplate geometry was characterized based
on vertebral level and endplate area. Bone quality was
characterized by patient age, gender, and BMD. End-
plates were left intact or were prepared for fusion by
perforation or burring.
Materials and Methods
A total of 28 fresh frozen human cadaveric cervical spines were
obtained through the willed body program at the University of
Michigan and the International Institute for the Advancement
of Medicine. Sixty percent were female. The average age at Figure 1. Diagram of the perforation pattern employed.
demise was 72 years (⫾ 14 years). Anteroposterior (AP) and
lateral radiographs were obtained to exclude lytic lesions or
other anomalies. A DEXA scan was then obtained to quantify test subjects were then loaded at a rate of 0.2 mm/s on an
mineral content. Average as well as level specific, lateral BMD Instron materials tester (Canton, MA (Figure 2). Endplate fail-
values were obtained using a Lunar DPXL system (Madison, ure was defined as reversal of the force-displacement curve
WI). After screening, 21 cadavers were selected for further wherein decreasing force was needed to further advance the
study. The remaining seven specimens were found to have prior rod. For the burred specimen, clear identification of the failure
cervical surgery, marked degeneration to the point of autofu- point was difficult. Each specimen was compressed to 5 mm.
sion, lytic lesions, or other anomalies. Failure was defined as that load at which the indenter advanced
Fifty-five vertebrae were harvested from the 21 spines. Lev- greater than 0.25 mm without further increase in load. A step-
els were randomly selected and included the inferior endplate wise linear regression was then used to compare failure load
of C2 to the superior endplate of T1. Please see Table 1 for with bone mineral density, gender, age, vertebral level, end-
individual specimen characteristics. Individual vertebrae were plate geometry, and endplate preparation technique.
separated, and all soft tissue was removed. Bony elements were
Results
left intact, including the posterior elements. The specimens
were then potted in a polyester resin to the approximate mid- Mean BMD in these specimens was 0.713 g/cm2 (⫾
point of the vertebral body in order to maintain a perpendicular 0.173 g/cm2). The male specimens had a greater mean
orientation of the upper endplate relative to the indenter. End-
plate geometry was calculated using a direct caliper measure-
ment of the outer vertebral width and length. Area was calcu-
lated assuming elliptical geometry.
The cartilage endplate was removed using a curette. Thirty-
five specimens were tested without additional endplate prepa-
ration (the intact specimen). Given that the indenter was stan-
dardized in size, the perforations were standardized relative to
the indenter, not the size of the vertebral endplate. Their con-
figuration was meant to simulate surface area for vascular in-
flow into the center (noncortical) portion of the strut graft. The
perforations were made with a 1-mm sharp, fine curette in a
square pattern centered on the middle of the docking site for
the indenter. The perforations were 3 mm apart (center to cen-
ter) (Figure 1). In the burred specimens, the entire visible end-
plate medial to the uncovertebral joints was gradually burred Figure 2. A polycarbonate rod was fashioned to simulate the
until the underlying trabecular bone became visible. geometry of an intervertebral strut graft. This was then used to
A 9 mm diameter (area 64 mm2) polycarbonate rod was compress into the vertebral endplate using an Instron materials
fashioned to simulate a typical intervertebral strut graft. The tester.
2206 Spine • Volume 28 • Number 19 • 2003

BMD (0.8133 ⫾ 0.201 g/cm2) than did the female (0.648


⫾ 0.114 g/cm2) (P ⫽ 0.0193). However, the male spec-
imens were also, on average, younger (66.2 vs. 75.8
years). Finally, males had a greater mean maximum com-
pressive failure load than females (911 vs. 650 N). Al-
though these differences are significant, we cannot com-
ment on which variable, age or gender, had the greater
impact in that the male specimens were also younger.
A mean 754 N (⫾ 445 N) force was required before
endplate failure occurred. In the intact specimen, failure
occurred abruptly (at a mean 897 N) as the cortical end-
plate gave way (Figure 3A). There was continued resis-
tance to rod advancement, however, through compres-
sion of the underlying cancellous bone. Perforated
specimens demonstrated a similar pattern of vertebral
penetration at a lower mean force, 590 N (Figure 3B).
Burred specimens exhibited a gradual failure with slow
impaction of the subendplate bone (Figure 3C). Failure
occurred with less force than in either the perforated or
intact specimens, at 403 N. Specimen age and BMD were
similar between the endplate preparation groups: intact
(72 years, 0.732 g/cm2), perforated (74 years, 0.681
g/cm2), and burred (70 years, 0.676 g/cm2).
A stepwise, univariate linear regression was used to
compare the point of endplate failure with the vertebral
level, endplate area, gender, age, BMD, and preparation
technique. A trend of increasing endplate failure load
was noted with increasing endplate area. Similarly, in-
creasing BMD was associated with increasing endplate
failure load, but significance was not reached. Increasing
age (P ⫽ 0.0203), vertebral level below C5 (P ⬍ 0.0001),
endplate burring (P ⫽ 0.0068), and female gender (P ⫽
0.0452) were associated with statistically significant
lower endplate compressive loads (Figures 4 and 5).

Discussion Figure 3. A, A typical load-displacement curve from a specimen in


We theorized that ultimate endplate compressive load which the endplate was left intact. That is, after cartilage removal,
no further perforation or burring was undertaken. In this specimen,
could be predicted based on three variables: endplate sudden failure of the endplate occurred at 650 N. This was fol-
geometry, bone quality, and endplate preparation tech- lowed by continued resistance to further compression by the
nique. Endplate geometry may affect stress distribution. subcortical trabecular bone. Failure is indicated by an “X.” End-
Axial force transmitted closer to the cortical rim of the plate failure loads were significantly different in each group. That
vertebral body may allow increased loads before end- is, intact endplates failed at a significantly higher load than did
perforated (P ⬍ 0.023). Similarly, perforated endplates failed at a
plate failure. However, in our study, endplate dimen- significantly higher load than did burred (P ⬍ 0.017). When intact
sions did not significantly predict the ability of the end- endplates are compared with burred endplates, the difference is
plate to resist failure when compressed with a great (P ⫽ 0.0068). B, A typical load-displacement curve of a
standardized, simulated strut graft. cervical endplate after perforation with a curette. Although this
Inferior bone quality, as measured by increasing age curve is similar to that of the intact endplate, the failure occurs at
a lower load, 418 N. Moreover, the loading curve does not dem-
and female gender, was associated with lower compres- onstrate the sharp demarcation noted with failure of the intact
sive loads at failure. Younger and male specimens had endplate. Failure is indicated by an “X.” C, A typical load-
stronger endplates as measured by higher endplate fail- displacement curve of a cervical vertebra after endplate removal
ure loads. Female gender may also affect vertebral geom- with a burr. In this case, a gradual increase in load occurs with
etry; however, this was not directly measured. Bone min- increasing displacement as the trabecular bone is compacted. A
discrete point of failure is difficult to identify, but was selected
eral density measures, via DEXA scanning, did not based on a 0.25 mm displacement without a significant increase in
predict endplate compressive loads in a statistically sig- load; in this example, 234 N. Failure is indicated by an “X.”
nificant manner. We feel that more accurate measures of
BMD in these spondylotic, elderly cadavers may have
produced significant results. Cervical DEXA lacks a
Cervical Endplate Compression Load • Truumees et al 2207

absolute thickness, is critical in load bearing. In Lim et


al’s study, a finite element model was used to assess the
effect of endplate perforation. These authors found that a
single, larger central perforation decreased endplate
strength less than multiple, smaller perforations. In our
study, we directly tested the effect of four small endplate
perforations. Although these perforations led to a signif-
icantly lower endplate failure load, this failure load was
significantly higher than that achieved after burring the
endplate. In clinical practice, we prefer not to create one
larger hole centrally because exact geometry and place-
ment of the intervertebral graft may vary. End-bearing of
the structural portion of the graft on the hole may lead to
subsidence. The size and distribution of smaller perfora-
Figure 4. The effects of increasing endplate violation on load at tions may be more easily altered from case to case as
failure. These differences were statistically significant.
bone quality and geometry dictate.
We compared endplate failure loads from our study
readily available, specific scanner protocol and may be and those of Lim et al with graft failure data from the
inaccurate in spondylotic specimens.10 reports by An et al, White and Hirsh, White et al, and
The method of preparation did significantly affect the Wittenberg et al.6,7,8,13 When loaded in compression,
endplates ability to withstand compressive loads. End- strut grafts were between 1.3 and 8 times stronger than
plate preparation, such as perforation and burring, are the intact endplate. Smith-Robinson grafts were 1.3 to
often used to encourage graft incorporation.11,12 How- 5.3 times stronger than the intact endplate. Strut grafts
ever, intact endplates failed at significantly higher loads were much stronger than burred endplates (5.4 to 12.6
than their perforated or burred counterparts. times). Smith Robinson grafts were from 2.8 to 8.4 times
Despite differences in experimental design, our values stronger than a burred endplate.
for endplate failure loads of intact and burred specimens In a separate study, we measured the compressive load
are similar to previously reported values.9 Our study dif- on a simulated Smith Robinson anterior cervical graft.14
fers from previous work in that the vertebrae were not The mean compressive load on a 6 mm graft loaded with
sectioned in the horizontal plane, but were tested intact. simulated head weight was 16.2 N. The intact endplate
Ours is the first study to directly measure the failure load withstood 55.4 times these measured loads. In the same
of perforated endplates. In our study, endplates were study, a larger, 8 mm graft was subjected to a compres-
compressed to a depth of 5 mm; this additional depth sive load of 29.2 N, or one-thirtieth of the intact endplate
was selected to ensure complete failure of our specimens. failure loads measured in this study. Burred endplates
Particularly in the burred specimens, variability in the were 13.8 to 24.9 times stronger than these ex vivo mea-
pattern of trabecular failure may lead to partial collapse surements of compressive load on 6 or 8 mm grafts. This
being falsely recorded as complete failure. study of anterior strut grafts simulated loading at the
Although Lim et al found that endplate thickness was time of graft insertion before postoperative graft com-
not directly related to failure load, greater degrees of pression due to muscle forces and neck flexion.
endplate burring did correspond to lower failure loads.9 Although in vivo cervical graft loads have not been
These findings imply that endplate integrity, rather than extensively described in the literature, Moroney et al and
others have estimated compressive loads on entire cervi-
cal motion segments using a mathematical model and
electromyograph (EMG) data.15 In flexion, the compres-
sive load at C4 –C5 was estimated at 558 N. This com-
pressive load was therefore less than the failure load of
an intact endplate (754 N). However, burred endplates
failed at lower compressive loads (403 N) than those
estimated based on EMG data. These endplates would
therefore be subject to failure and graft subsidence. In
our study, perforated endplates fail at only slightly
higher loads (590 N vs. 558 N) than those estimated by
Moroney et al.
Our study is limited by its ex vivo assessment of bone
strength. The differences in mechanical properties of
bone in vivo are not known. Our use of a polycarbonate
Figure 5. Male endplates fail at a higher mean load than female. indenter only approximates axial force delivered by a
This difference was statistically significant. strut graft in an anterior cervical fusion. Moreover, dur-
2208 Spine • Volume 28 • Number 19 • 2003

ing the initial period of graft incorporation, vascular in- Supervisor, Department of Nuclear Medicine, William
growth is associated with a decrease in mechanical Beaumont Hospital.
strength. Later, this strength returns.16 Our model esti-
mates failure load at the time of surgery only. Ultimately,
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