Abstract
Background: Surgical treatment of rotator cuff tears may be
complicated by osteoporosis of the proximal part of the humerus. The purpose
of this study was to determine whether pullout strength of suture anchors is
affected by the location of the anchor placement and by bone mineral density.
We hypothesized that higher bone mineral density is associated with higher
pullout strength of suture anchors.
Methods: Peripheral quantitative computed tomography was used to
measure total, trabecular, and cortical bone mineral density in different
regions of the lesser and greater tuberosities in seventeen cadaveric humeri.
Suture anchors were inserted into individual regions and subjected to cyclic
loading. Repeated-measures analysis of variance was used to assess differences
in bone mineral density and load to failure between regions of interest.
Pearson correlation was used to determine the association between bone mineral
density and pullout strength of suture anchors.
Results: Total, trabecular, and cortical bone mineral densities were
an average of 50%, 50%, and 10% higher, respectively, in the proximal part of
the tuberosities compared with the distal part (p < 0.01). Within the
proximal part of the greater tuberosity, trabecular bone mineral density of
the posterior region and cortical bone mineral density of the middle region
were, on the average, 25% and 16% higher, respectively, than the densities in
the other regions (p < 0.01). Load to failure in the proximal part of the
tuberosities was an average of 53% higher than that in the distal part (p <
0.01). The lesser tuberosity showed, on the average, a 32% higher load to
failure than did the greater tuberosity (p < 0.01). Within the proximal
part of the greater tuberosity, loads to failure in the anterior and middle
regions were, on the average, 62% higher than the load to failure in the
posterior region (p < 0.01). Overall positive correlations were found
between bone mineral density and load to failure (0.65 = r = 0.74, p
< 0.01).
Conclusions: We found that pullout strength of suture anchors
correlates well with bone mineral density of the tuberosities. Higher loads to
failure were found in regions in the proximal part of the tuberosities.
Placement of anchors in these regions may prevent anchor loosening, formation
of a tendon-bone gap, and failure of the rotator cuff repair.
Rotator cuff tears are common injuries in patients over sixty years of
age1. These patients
can also have osteoporosis of the proximal part of the humerus, which can be
aggravated by chronic progression of a rotator cuff
tear2-6.
Three major factors determine the success of a rotator cuff repair: suture
material, tendon-grasping technique, and tendon-to-bone
fixation5,7.
With advances in arthroscopic surgery, the use of suture anchors has become
more popular because of the ease and speed of their use and because of the
decreased surgical exposure and
morbidity8-10.
Rotator cuff repairs with suture anchors and transosseous sutures were
found to have high fixation strength in experimental
studies5,7,10-13.
However, the applicability of these findings might be limited since most of
the studies were performed in porcine specimens, which are not representative
of human bones. Furthermore, we are not aware of any studies that have
accounted for bone density changes in elderly patients. In such patients, the
strength of rotator cuff repairs might be compromised by a decrease in bone
quality, resulting in suture anchors pulling out of bone and transosseous
sutures cutting through bone before the tendon
heals5,7,14,15.
In biomechanical studies performed on human humeri, rotator cuff repairs
frequently have failed at the bone
interface9,14,16,17.
Djurasovic et al. reported, in a clinical study, that eight of eighty patients
needed surgical revision of a rotator cuff repair because of migration and
loosening of suture
anchors18.
Barber et al.7
and Goradia et
al.19 attempted to
correlate the bone quality of the humeral head with the pullout strength of
suture anchors. Those investigators used two-dimensional dual-energy x-ray
absorptiometry to study the bone mineral density of the proximal part of the
humerus. Barber et al. found pullout strength in the anterior part of the
greater tuberosity (96 N) to be 40% lower than that in the posterior part (160
N). Neither study showed a significant difference in total bone mineral
density among the various regions of the greater tuberosity, and no
correlation was seen between pullout strength of suture anchors and total bone
mineral density. The two-dimensional dual-energy x-ray absorptiometry
technique used in those studies allowed measurement of only total bone mineral
density; it was not possible to discriminate between trabecular and cortical
bone mineral
density7,19.
Current anchor designs may vary with regard to the type of bone on which
they rely for fixation. For example, hook-like anchors may rely more on a
strong cortical layer of the humeral head, whereas the pullout strength of
screw-like anchors may be affected by both trabecular and cortical
bone7. Therefore, a
more systematic analysis of three-dimensional bone mineral density and its
cortical and trabecular distribution may be needed to identify a potential
association between the bone mineral density of the humeral head and the
pullout strength of suture anchors. The purpose of this study was to
quantitatively assess total, trabecular, and cortical bone mineral density of
clinically relevant regions within the greater and lesser tuberosities and to
determine whether there was a relationship between pullout strength, the
location of anchor placement, and bone mineral density. We hypothesized that
higher bone mineral density of the humeral head region was associated with
higher pullout strength of suture anchors.
Preparation of Specimens
Twenty unpaired fresh-frozen human humeri were harvested and were stored at
—20°C. The specimens were thawed at room temperature for twenty-four
hours before testing. After thawing, they were dissected and all soft tissue
was removed. All specimens had a macroscopically intact rotator cuff. Biplanar
radiographs were used to identify bone abnormalities. Specimens with a
previous proximal humeral fracture, underlying pathologic changes, or evidence
of surgical intervention were excluded. Three specimens were excluded on the
basis of these criteria, and seventeen specimens (twelve from male donors and
five from female donors, with a mean age of seventy years [range, fifty-nine
to ninety-eight years] at the time of death) were included in the study.
Bone Mineral Density of the Greater and Lesser Tuberosities
The total, trabecular, and cortical bone mineral density of the greater and
lesser tuberosities was measured with use of peripheral quantitative computed
tomography (XCT-960A; Norland/Stratec, Fort Atkinson,
Wisconsin)20,21.
For these measurements, each humerus was fixed horizontally in a custom-made
jig with the lesser tuberosity in the twelve o'clock position
(Fig. 1). Axial scans of each
specimen were made to determine bone mineral density (pixel size, 0.59 mm;
slice thickness, 2.5 mm; slice separation, 2 mm). The inferior border of the
humeral head was determined by a horizontal line running through the lowest
point of the articular surface. All computed tomography scans were performed
and analyzed by the same investigator.
On the cross-sectional view, four specific regions of interest were
determined on the middle computed tomography image of the humeral head. A
diagonal line separated the articular surface from the tuberosities, and a
second line, running though the center of the bicipital groove, separated the
lesser from the greater tuberosity (Fig.
1). The greater tuberosity was divided into three regions of
interest: anterior (GTa), middle (GTm), and posterior
(GTp) (Fig. 1).
These regions of interest were copied automatically to each image of the same
specimen. An average of nineteen images was made for each specimen, with a
range of sixteen to twenty-three images, depending on the size of the humeral
head.
The humeral head was divided into four slices of the same height, which
were designated, from proximal to distal, as slice1 through
slice4 (Fig. 2). The
total and trabecular areas of the anterior, middle, and posterior regions of
the greater tuberosity and of the lesser tuberosity were contoured manually on
the middle computed tomography image of slice1 through
slice4. When the total area was contoured for the anterior region
of the greater tuberosity and for the lesser tuberosity, the cortical bone of
the bicipital grove was excluded because suture anchors are not usually
inserted in that location. All contouring was performed by the same
investigator, who following a standardized pre-hoc protocol. The coefficient
of variation for determining the bone mineral density of the specific regions
of interest was <3% (0.7% for total bone mineral density, 0.8% for
trabecular bone mineral density, and 2.7% for cortical bone mineral density).
Automatic determination of these parameters was not possible as the software
was not capable of distinguishing between cortical and trabecular bone in
regions that were not completely surrounded by cortical bone. Total and
trabecular bone mineral density and bone mineral content were determined
separately for the proximal (slice1 + slice2) and distal
(slice3 + slice4) parts of each region of interest. The
cortical bone mineral density was calculated on the basis of the difference
between the total and trabecular volumes and the difference between the total
and trabecular bone mineral contents.
Pullout Tests of Suture Anchors
Following peripheral quantitative computed tomography scanning, each
proximal humeral specimen was potted in polymethylmethacrylate approximately
10 mm below the distal border of the humeral head. To ensure that our manually
defined regions of interest on each humeral head were identical to the
corresponding regions of interest on the peripheral quantitative computed
tomography scans, we followed a strict, standardized protocol. The inferior
border of the humeral head was defined as the lowest point of the articular
surface and was marked with a horizontal line on each specimen
(Fig. 3). The border between
the proximal and distal parts of the humeral head was determined with digital
calipers (Mitutoyo, Tokyo, Japan; measurement error, ±0.02 mm) and
marked with a horizontal line (proximal-distal line). A vertical line running
through the interface of the proximal-distal line with the anterior border of
the articular surface marked the anterior border of the lesser tuberosity, and
a vertical line running through the interface of the proximal-distal line and
the posterior border of the articular surface determined the posterior border
of the greater tuberosity. A line running through the deepest point of the
bicipital groove on the proximal-distal line separated the greater from the
lesser tuberosity. With use of a tape measure with 1-mm subdivisions, the
greater tuberosity was divided into six regions: proximal anterior
(GTpa), proximal middle (GTpm),
proximal posterior (GTpp), distal anterior
(GTda), distal middle (GTdm), and
distal posterior (GTdp)
(Fig. 3, A). The
lesser tuberosity was divided, in the same manner, into two regions: proximal
(LTp) and distal (LTd)
(Fig. 3, B).
Metal screw-like suture anchors (5-mm Fastin RC; Mitek, Norwood,
Massachusetts) were placed in the proximal and distal parts of each region of
interest. Proximal anchors were placed in the middle between the articular
surface and the tip of the greater or lesser tuberosity. Distal anchors were
inserted 10 to 15 mm distal to the tip of the greater or lesser tuberosity, in
the center of the distal part of each region of interest. Anchors were
inserted at a 45° angle to the bone surface
(Fig.
4)22.
We used self-tapping metal screw-like anchors. According to the manufacturer's
recommendations, the anchors were inserted into the bone without predrilling a
pilot hole. To exclude any interference when the pullout testing was
performed, the distance between the sites of anchor insertion was at least 10
mm, as recommended
previously17,23.
Since we were investigating the relationship between pullout strength of
suture anchors and bone quality, the original sutures were replaced by
0.62-mm-diameter steel wire (McMaster-Carr Supply, Chicago, Illinois) to
eliminate suture breakage as a mode of
failure10. The
proximal part of the humerus was then fixed in a customized jig. The steel
wire was secured in a handmade clamp, with a distance of 40 mm between the tip
of the anchor and the clamp. The clamp was connected to a materials testing
machine (Bionix 200; MTS Systems, Eden Prairie, Minnesota), and the humeral
head was oriented in such a way that load was applied parallel to the axis of
anchor insertion10.
This testing setup was previously established in a number of studies by Barber
et al., and it simulates the worst-case scenario for failure strength of
suture
anchors10-12.
Anchors were cyclically loaded with a preload of 4 N and an extension rate
of 1 mm/sec. A 50-N maximum load was chosen for the first ten cycles, and this
was increased in 50-N increments after each ten cycles. A maximum of forty
cycles was performed (maximum load, 200 N). Linear load to failure was then
applied to the anchors that had not pulled out after forty cycles. For each
pullout test, the load to failure, number of cycles completed, and stiffness
of the anchor fixation were determined. Real-time data acquisition was
performed with use of TestWorks (version 4.04 B; MTS Systems). Load-elongation
data for each anchor in each region of interest were recorded. Stiffness was
calculated for cycles ten, twenty, thirty, and forty according to the slope of
the load-elongation curve between the 10% and 90% points of the maximum
load.
Statistical Analysis
A power analysis indicated that a sample size of seventeen specimens would
provide statistical power of 86% to detect mean differences in load to failure
of one standard deviation between the regions of interests of the lesser and
greater tuberosities (ß = 0.1, a = 0.01). The Kolmogorov-Smirnov
test was used to evaluate whether load to failure and bone mineral density
followed a normal (gaussian-shaped) distribution, and no significant
departures were
identified24.
Repeated-measures analysis of variance was used to compare load to failure and
bone mineral density between regions of interest. The stiffnesses of the
anchor fixation were compared between the proximal and distal parts of the
tuberosities with use of paired t tests. A two-tailed t test (p < 0.01) was
chosen a priori to declare a significant result, to account for multiple
comparisons25,26.
The Pearson product-moment correlation coefficient (r) was calculated to
evaluate the linear association between bone mineral density and load to
failure. Stepwise multiple linear regression analysis was used to determine
whether cortical and trabecular bone mineral density were significant
predictors of load to failure and number of completed cycles with respect to
each region of interest within the proximal and distal parts of the humeral
head24. Prediction
equations were derived on the basis of the significant variables in the final
stepwise models. Data analysis was performed with use of the SPSS statistical
package (version 11.0; SPSS, Chicago, Illinois). Power calculations were
determined with use of the nQuery Advisor software package (version 4.0;
Statistical Solutions, Boston, Massachusetts). Continuous data are presented
as means and standard deviations.
Differences in Bone Mineral Density Between the Proximal and Distal
Regions of Interest
The proximal part of the tuberosities had higher total, trabecular, and
cortical bone mineral densities than the distal part (p < 0.01) (Figs.
5 and
6;
Table I). Within the lesser
tuberosity, total and trabecular bone mineral densities were higher in the
proximal part than they were in the distal part (p < 0.01), but there was
no significant difference between the proximal and distal regions with regard
to cortical bone mineral density (p = 0.70). In addition, the proximal part of
the greater tuberosity showed higher total, trabecular, and cortical bone
mineral densities than did the distal part (p < 0.01). All regions of
interest (anterior, middle, and posterior) in the greater tuberosity showed
higher total and trabecular bone mineral densities in the proximal part than
in the distal part, whereas cortical bone mineral density was higher in the
proximal part than in the distal part only in the middle region of the greater
tuberosity (p < 0.01).
Differences in Trabecular and Cortical Bone Mineral Densities Between
Regions of Interest
The proximal part of the greater tuberosity showed a higher trabecular and
a lower cortical bone mineral density than did the proximal part of the lesser
tuberosity (p < 0.01) (Fig.
5). No difference in trabecular bone mineral density was found
between the distal parts of the greater and lesser tuberosities (p = 0.71),
but cortical bone mineral density was higher in the distal part of the lesser
tuberosity than in the distal part of the greater tuberosity (p < 0.01)
(Fig. 6). Within the proximal
part of the greater tuberosity, trabecular bone mineral density was higher in
the posterior region than in the anterior region or the middle region (p <
0.01). Within the distal part of the greater tuberosity, trabecular bone
mineral density was higher in the posterior region than in the middle region
(p < 0.01). Furthermore, within the proximal part of the greater
tuberosity, cortical bone mineral density was higher in the middle region than
in the posterior region or the anterior region (p < 0.01). Finally, within
the distal part of the greater tuberosity, cortical bone mineral density was
higher in the anterior region than in the posterior or middle region (p <
0.01).
Pullout Strength of Suture Anchors in Specific Regions of
Interest
The proximal part of the tuberosities demonstrated a higher load to failure
and number of cycles than did the distal part (p < 0.01)
(Table II). In addition, in
both the lesser and the greater tuberosity, the load to failure and the number
of cycles were higher in the proximal part than in the distal part (p <
0.01). Within the greater tuberosity, load to failure was higher in the
proximal middle region and proximal anterior region compared with their
respective distal parts (p < 0.01), whereas no significant difference was
detected between the proximal posterior and distal posterior regions.
Anchors inserted into the proximal and distal parts of the lesser
tuberosity showed higher loads to failure than those placed in the greater
tuberosity (p < 0.01) (Table
II). Within the proximal part of the greater tuberosity, load to
failure was higher in the anterior and middle regions than it was in the
posterior region (p < 0.01). Within the distal part of the greater
tuberosity, no significant differences in load to failure were seen among the
anterior, middle, and posterior regions.
Stiffness of the Anchor Fixation
The stiffnesses of the anchor fixation did not differ significantly between
the proximal and distal parts of the tuberosities at 50 N (44 ± 5 N/mm
compared with 45 ± 6 N/mm, respectively), 100 N (94 ± 8 N/mm
compared with 92 ± 9 N/mm), 150 N (137 ± 9 N/mm compared with
130 ± 12 N/mm), or 200 N (166 ± 15 N/mm compared with 158
± 12 N/mm) (all p > 0.10, paired t tests). At 200 N, the stiffness
value was based on only eight specimens, since the majority of the anchors
failed at lower loads. In addition, no differences in stiffness were found
between the greater and lesser tuberosities or between any other regions of
interest.
Correlation Between Bone Mineral Density and Pullout Strength
There was a significant correlation between each of the bone mineral
density parameters (total, trabecular, and cortical) and load to failure. The
highest correlation was between total bone mineral density and load to failure
(correlation coefficient: r = 0.74, p < 0.01), but trabecular bone mineral
density (correlation coefficient: r = 0.71, p < 0.01) and cortical bone
mineral density (correlation coefficient: r = 0.65, p < 0.01) also had a
significant positive correlation with load to failure.
Regression Modeling of Loads to Failure
In the proximal part of the greater tuberosity, cortical bone mineral
density was a significant multivariate predictor of load to failure in the
greater tuberosity (t = 2.84, p = 0.012), in the anterior region of the
greater tuberosity (t = 2.63, p = 0.018), and in the posterior region of the
greater tuberosity (t = 4.16, p < 0.001 for cortical and trabecular bone
mineral density). In the distal part of the greater tuberosity, trabecular
bone mineral density was a significant multivariate predictor of load to
failure in the greater tuberosity (t = 3.08, p = 0.008) and the posterior (t =
2.63, p = 0.019), middle (t = 3.53, p = 0.003), and anterior (t = 2.75, p =
0.015) regions of the greater tuberosity.
In the proximal part of the lesser tuberosity, trabecular bone mineral
density was a significant multivariate predictor of load to failure (t = 4.76,
p < 0.001). In the distal part of the lesser tuberosity, cortical bone
mineral density was a significant multivariate predictor of load to failure (t
= 2.43, p = 0.028).
Table III shows fitted
regression models for prediction of load to failure by cortical and trabecular
bone mineral density in each region of interest.
Poor fixation of suture anchors due to reduced bone quality of the proximal
part of the humerus is a major problem in rotator cuff
repair4,5,7,9,14,17,18.
Pullout of suture anchors before tendon-healing may result in gap formation
between the tendon and the bone, rupture of the rotator cuff repair, and a
poor
outcome4,5,7,14,19.
Recommendations in the literature regarding the optimum region for placement
of suture anchors in rotator cuff repair are
controversial8,13,19,27,28.
Surgeons are limited to the region of the greater and lesser tuberosity when
reattaching the torn rotator cuff. The site of tendon reattachment is
influenced by the size of the rotator cuff tear, the involved rotator cuff
tendons, the degree of tendon retraction, and the amount of tendon
mobilization achieved as well as the degree of tendon tension during the
rotator cuff
surgery8,27,28.
However, within these limitations, the surgeon still has some options
regarding where to reaffix the torn rotator cuff. In an experimental study,
Rossouw et al. found that suture anchors placed 25 mm distal of the tip of the
greater tuberosity had higher pullout
strengths13. The
authors speculated that a higher cortical thickness might be the reason for
this increase in pullout strength and therefore recommended insertion of
anchors as far distal from the tip of the greater tuberosity as possible.
Furthermore, some review articles have recommended placing suture anchors
lateral and distal to the greater tuberosity because the bone stock was
thought to be better in that
area8,27.
In contrast, in other studies, a position medial to the tip of the
tuberosities was thought to be favorable for insertion of suture
anchors19,28.
Previous pullout tests of suture anchors in human proximal humeral
specimens showed the loads to failure to be only between 90 and 180
N5,7.
We found higher loads to failure, averaging 240 N and ranging from 173 to 333
N, depending on the bone site where the anchors had been inserted. The higher
pullout forces in our study might be attributed to differences in anchor
design and the way in which loads were applied. Load to failure was determined
with cyclic testing rather than linear pullout because cyclic testing is a
more physiologic approach of assessing loads applied to the rotator cuff
following
repair9,28.
We found a significant correlation between bone mineral density and the
pullout strength of suture anchors. Regression modeling of load to failure
showed cortical bone mineral density to be a better predictor of pullout
strength in the proximal part of the greater tuberosity than trabecular bone
mineral density, whereas trabecular-bone mineral density was a
better predictor of load to failure in the distal part of the greater
tuberosity. When only total bone mineral density is analyzed, the correlation
between bone mineral density and pullout strength is not that obvious because
total bone mineral density is a combination of trabecular and cortical bone
mineral density. This would explain the findings of Barber et
al.7 and Goradia et
al.19, who
investigated the correlation between total bone mineral density and pullout
strength and found no correlation between them.
We investigated the effect of bone mineral density on the pullout strength
of a metal screw-like suture anchor. However, other anchors that differ in
material, size, and design are currently available for rotator cuff repair,
and they may have shown different failure patterns and loads to
failure7,19.
Also, the association between bone mineral density and the pullout strength of
other anchor types, such as hook-like suture anchors, might differ from the
correlations found in our study. We chose the metal screw-like anchor because
it is one of the most commonly used anchors.
In the past, creation of a cancellous trough during rotator cuff repair was
recommended to improve tendon-to-bone
healing29. However,
in 1995, St. Pierre et al. demonstrated, in a biomechanical and histological
study, that there is no significant benefit to creating this trough to expose
tendon to cancellous
bone30. Shoulder
surgeons use different methods to attach the rotator cuff to bone. When
performing arthroscopic repairs, most surgeons abrade the bone surface at the
attachment site for the rotator cuff, rather than removing the cortical bone
and creating a trough in the cancellous
bone7,9,19,23,27,31.
Therefore, in our experimental model, cortical bone was not removed and no
cancellous trough was created before anchor placement.
In addition to bone mineral density, other parameters such as trabecular
microarchitecture of bone may affect the pullout strength of suture
anchors7. Insertion
of anchors at a 45° angle to the bone surface is recommended in clinical
situations, as this is perpendicular to the direction of rotator cuff
pull22. Therefore,
we inserted the anchors at a 45° angle in our experimental model, to
ensure the same trabecular alignment as is present in clinical situations.
However, the direction of pull during testing was parallel to the axis of the
suture anchor, since this simulates the worst-case scenario of failure
strength. These testing conditions were previously established and justified
by a number of studies by Barber et al., who investigated the bone-anchor
interface7,10-12.
Nevertheless, one might speculate that pullout strength is higher when anchors
are tested perpendicular to the insertion angle, especially when the anchors
were inserted distal to the tip of the greater or lesser tuberosity, but this
scenario was not evaluated in our model. In our study, all of the anchors
failed by pulling out of the bone; we did not observe any bone fractures or
wire breakage. This mechanism of failure might differ from that observed on
testing of whole rotator cuff repair constructs or when biodegradable anchors
are used. The mode of failure in those situations could include anchor-eyelet
cutout, suture breakage, or tendon
slipping9,10,19.
Since the main goal of this project was to investigate the relationship
between bone mineral density and anchor pullout strength, simulation of other
failure modes was beyond the scope of the study.
In conclusion, we recommend insertion of suture anchors medial to the tip
of the greater tuberosity and particularly in the proximal-anterior and
proximal-middle regions, which provide the best bone stock. We cannot confirm
the previous suggestions that there is better cortical bone stock and higher
anchor pullout strength distal to the tip of the greater tuberosity. Placement
of anchors in the regions that we recommended would provide stronger fixation
within the tuberosities and may prevent anchor loosening, formation of a
tendon-bone gap, and failure of the rotator cuff repair.
Note: The authors acknowledge the continuous assistance of Dr.
Bouxsein throughout this study.
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