Abstract
Background: Bone-healing is known to be sensitive to the mechanical
stability of fixation. However, the influence on healing of the individual
components of fixation stiffness remains unclear. The aim of this study was to
investigate the relationship between the initial in vitro fixation stiffness
and the strength and stiffness of the callus after nine weeks. We hypothesized
that axial stiffness would determine the healing outcome.
Methods: A standardized midshaft osteotomy of the right tibia was
performed on Merino-mix sheep and was stabilized with either one of four
monolateral external fixators or one of two tibial nails inserted without
reaming. The in vitro stiffness of fixation was determined in six loading
conditions (axial compression, torsion, as well as bending and shear in the
anteroposterior and mediolateral planes) on ovine tibial specimens. Stiffness
was calculated by relating displacements of the fracture fragments, determined
by means of attached optical markers, and the loads applied by a materials
testing machine. Torsional testing until failure of the explanted tibiae was
performed with use of a standard materials testing machine after nine weeks of
healing to determine the failure moment and the torsional stiffness of the
healed tibia.
Results: External fixation in sheep generally resulted in higher
fixation stiffness than did conventional unreamed tibial nailing. The use of
angle-stable locking screws in tibial nailing resulted in fixation stiffness
comparable with that of external fixation. The highest torsional moment to
failure was observed for the external fixator with moderate axial stiffness
and high shear stiffness. The fixator with the highest axial stability did not
result in the highest failure moment. Low axial stability in combination with
low shear stability resulted in the lowest failure moment.
Conclusions: In this study, a clear relationship between the
stability of fixation and the mechanical strength of the healing tibia was
seen. Moderate levels of axial stability were associated with the highest
callus strength and stiffness.
Clinical Relevance: Optimizing axial stability and limiting shear
instability appear to be important for creating conditions for timely
fracture-healing.
Osteosynthesis devices are commonly utilized in the treatment of fractures
to stabilize the fracture fragments until union occurs. Depending on the
location and the type of fracture and the extent of soft-tissue damage, the
indication for the use of a particular osteosynthesis device may vary. For
fractures in the diaphyseal region of the tibia, fixation with a monolateral
external fixator or an intramedullary nail is
common1. Circular
external (Ilizarov) fixation devices provide an additional treatment
alternative for challenging
fractures2.
Regardless of the choice of osteosynthesis device, the healing of long-bone
fractures is influenced by the mechanical fixation stability that is
achieved3-5.
Mechanical testing of healed bones has demonstrated that the mechanical
strength and stiffness of the fracture callus is related to the degree of
fixation
stability6-9.
The differentiation and proliferation of callus tissue has been shown to be
dependent on the local mechanical conditions, among other
factors10,11.
The mechanical conditions in the healing callus tissue are related to the
interfragmentary movements, which in turn are a function of fixation stability
and
limb-loading12,13.
While moderate axial interfragmentary movements have been shown to be
stimulatory for healing, the influence of interfragmentary shear movements on
healing is not so
clear3,14-16.
As a consequence, clear clinical guidelines on the stiffness of osteosynthesis
that is necessary to optimize the treatment of long-bone fractures have been
elusive.
Previous studies investigating the influence of mechanical stability on
bone-healing have typically addressed the influence of axial
stability12,17-19.
Alternatively, studies have investigated the influence of fixation systems
that produce either pure axial compression or interfragmentary shear by
developing special fixation devices that only allow specific modes of
interfragmentary
movement15,16.
The monitoring of patients, however, has demonstrated that the fixation
systems in clinical use create complex load situations resulting in a mixture
of axial compression, translational shear, bending, and axial
torsion13,20,21.
Because of the highly nonlinear nature of fracture fixation systems and the
complex loading, it is difficult to predict interfragmentary movements in vivo
on the basis of in vitro fixation stiffness
alone22,23.
It is therefore essential to define boundaries of fixation stability for
optimal healing on the basis of both clinically relevant fixation and loading
conditions. With use of previously developed methods, it has been possible to
determine in vitro the fixation stiffness of osteosynthesis devices in six
degrees of freedom: three translations and three
rotations24. In
addition, biomechanical testing has been applied to determine the torsional
strength and stiffness of healing calluses after nine weeks of
healing25. The aim
of this study was to investigate the relationship between initial in vitro
fixation stiffness and the strength and stiffness of the callus after nine
weeks. We hypothesized that the axial stiffness component of the fixator would
determine the healing outcome.
Fixation Devices
Six fixation devices were investigated
(Fig.
1)23,25-27.
They included: (1) A medially mounted monolateral external fixator (Synthes,
Bochum, Germany), which consisted of six Schanz screws (5 mm in diameter) and
two carbon fiber rods (10 mm in diameter). The distance between the skin and
the inner rod was 5
mm25. (2) An
anteromedially mounted monolateral external fixator (Synthes), which was the
same as the medially mounted monolateral external fixator but was mounted
anteromedially. The distance between the skin and the inner rod was 5
mm25. (3) A rigid
monolateral external fixator (Synthes), which consisted of six Schanz screws
(5 mm in diameter) and two steel rods (10 mm in diameter) mounted medially.
The distance between the skin and the inner rod was 15
mm23. (4) A
semirigid monolateral external fixator (Synthes), which was similar to the
rigid system except a custom-made sliding joint was placed in the middle of
the inner rod to decrease stability. The distance between the skin and the
inner rod was 10
mm23. (5) An
unreamed tibial nail (UTN, number 479.250; Synthes), which was a commercially
available 9-mm-diameter tibial nail that was shortened to fit the sheep tibia.
The nail was secured with four 3.9-mm-diameter mediolateral locking bolts
(number 458.200-800;
Synthes)26. (6) An
angle-stable tibial nail (Synthes, Oberdorf, Switzerland), which was an
unreamed tibial nail that was modified to have smaller, threaded locking
holes. The threads of the locking holes corresponded to the threads of
commercially available 3.9-mm-diameter titanium locking bolts, such that the
bolts fitted into the locking holes
exactly27.
Animals, Surgical Procedure, and Care
Skeletally mature, healthy Merino-mix sheep (2.5 to 3.5 years old and with
a mean weight [and standard deviation] of 63 ± 8 kg) were divided into
six groups of eight animals each. The operations were performed with the
animals under general anesthesia and in aseptic conditions. All experiments
were carried out according to the policies and principles established by the
Animal Welfare Act, the National Institutes for Health Guide for Care and Use
of Laboratory Animals, and the National Animal Welfare Guidelines and were
approved by the local legal representative (Landesamt für Arbeitsschutz,
Gesundheitsschutz und technische Sicherheit, Berlin: registration number G
0188/99, G 0224/01, and G 0079/03).
All sheep underwent a standardized midshaft osteotomy of the right tibia,
which was performed at a defined distance from the medial malleolus with an
oscillating saw and distracted to 3 mm with the aid of a spacer tool. In all
cases, the soft tissue was preserved to exclude the influence of tissue damage
on the healing process and establish standardized experimental conditions. The
skin was sutured, and the shank was covered with a tube bandage. The osteotomy
of the tibial diaphysis was stabilized with either a monolateral external
fixator (medially mounted, anteromedially mounted, rigid, or semirigid) or an
unreamed tibial nail (a standard unreamed tibial nail or an angle-stable
tibial nail).
All external fixators were attached to the medial aspect of the right tibia
by placing the Schanz screws perpendicular to the subcutaneous cortex of the
bone, with the exception of the anteromedially mounted external fixator, which
was mounted on the anteromedial aspect. The Schanz screws were reproducibly
placed in all animals with use of a drill-guide, which also avoided
pre-bending of the screws.
Nail fixation was performed on the right tibia with the insertion point on
the anterior part of the tibial plateau, with an approach medial to the
patellar tendon. The capsule of the knee joint was not opened. After
conventional insertion, all nails were locked with mediolateral bolts, two
proximal and two distal. To model a clinically relevant surgical setting, the
locking bolts for the standard tibial nails were inserted proximally with a
standard aiming device and distally under radiographic control. The
radiographically controlled method was not sufficiently accurate for the
placement of distal interlocking screws of the angle-stable tibial nails.
Thus, a custom-made aiming device was used to locate both the proximal and the
distal locking-bolt holes. All wounds were closed in layers and were covered
with spray dressing, sterile compresses, and elastic conforming bandages.
An analgesic (flunixin meglumine; Finadyne) was administered for seven days
postoperatively to all animals. Daily animal care involved cleaning the
insertion points of the Schanz screws of the external fixator with
ethacridinlactate (Rivanol). A nine-week healing period was chosen. It has
been previously shown in sheep that osseous bridging is to be expected at
eight to nine
weeks12.
Craniocaudal radiographs were made immediately postoperatively and then at
weekly intervals.
Determination of in Vitro Fixation Stiffness
With use of a previously established
protocol24, which
is only briefly summarized in the present study, the stiffness of each type of
osteosynthesis was determined in vitro. The fixation device was implanted in
unpaired ovine tibial specimens (six per construct type) with use of the
surgical procedures described for the in vivo study. Leaving the tibial
muscles in place, the proximal and distal ends of the tibia were potted in
polymethylmethacrylate and were mounted by means of a custom-made jig in a
Zwick-1445 materials testing machine (Ulm, Germany). All bone-implant
constructs were tested in six loading conditions (axial compression, torsion,
bending in two planes, and shear in two planes) with use of the custom-made
jig24
(Fig. 2). Interfragmentary
movements, determined by means of attached optical markers, were recorded and
correlated to the applied loads to determine the stiffness of the fixation
construct. The axial stiffness, the shear and the bending stiffness in the
anteroposterior and mediolateral directions, together with the torsional
stiffness were calculated for each bone-implant construct. Finally, the
stiffness in each direction for each type of implant was averaged across the
six specimens.
Biomechanical Testing of Healed Tibia
All animals were killed nine weeks after surgery, at which point the
external fixators were removed and the intramedullary nails extracted. Both
the left and right tibiae were dissected, leaving only the muscles attached to
the tibia in place. For biomechanical testing, the tibial muscles were covered
with a bandage moistened with 0.9% saline solution. The proximal and distal
ends of each tibia were embedded in acrylate (Beracryl; W. Troller, Fulenbach,
Switzerland). With use of a Zwick-1445 materials testing machine, torsional
loading was applied until failure according to a previously described
procedure25. The
torsional stiffness was determined from the linear portion of the
load-deformation curve by dividing the change in torque by the change in
angular deformation. The torsional strength was taken as the maximum torque at
failure. The torsional stiffness and torsional strength were reported as a
percentage of that of the intact, contralateral side.
Relationship Between Failure Moment and Fixation Stability
The relationship between the fixation stability and the strength of the
healing callus was investigated by plotting the six components of in vitro
fixation stiffness against the torsional moment to failure of the healed
tibiae. With use of a least-squares approach, a linear or polynomial best fit
of the data was investigated. To examine the interaction between the axial and
shear components of fixation stiffness, the axial compressive stiffness was
plotted against the resultant shear stiffness. The resultant shear stiffness
was determined from the square root of the sum of the squares of the shear
stiffness components in the anteroposterior and mediolateral directions.
Contours were then sketched into the plot to indicate regions with a similar
moment to failure.
Statistical Analyses
The Kruskal-Wallis test was used to determine the similarity of the medians
of multiple groups. Thereafter, selected pairwise comparison, based on the
results of Kruskal-Wallis tests and examination of the box plots, was
performed with use of the Mann-Whitney U test for unpaired nonparametric data
(SPSS 12.0; SPSS, Chicago, Illinois). The level of significance was set at
0.05 and was corrected according to the Bonferroni-Holm test procedure. Curve
fitting was performed with use of regression analysis (least squares) to
determine the type of relationship that best fit the data.
Radiographic Results
In five of the fixator groups, a bridging periosteal callus could be seen
radiographically at nine weeks; the exception was the medially mounted
external fixator group where a gap was still visible
(Fig. 3). A large periosteal
callus could be seen in the semirigid group, and the cortices appeared not to
have completely bridged. In the unreamed tibial nail group, the osteotomy gap
was clearly visible in some specimens indicating no mineral bridging of the
gap. In contrast to the unreamed tibial nail group, healing in the group that
received the anglestable tibial nail was advanced and the original site of the
osteotomy was no longer clearly visible.
Fixation Stability
The axial compressive stiffness of the medially mounted external fixator (p
= 0.078, a = 0.025, Bonferroni corrected) and anteromedially mounted
external fixator groups (p = 0.065, a = 0.0167, Bonferroni corrected)
tended to be larger than the unreamed tibial nail group; the differences,
however, were not significant (Table
I, Fig. 4). The
value of compressive stiffness of the angle-stable nail was larger than that
for the standard unreamed tibial nail, but the difference was not significant
(p = 0.093, a = 0.05, Bonferroni corrected). Because of the large
variances within the groups, no significant difference was found between the
group medians (Kruskal-Wallis test, chi square = 9.367, 5 degrees of freedom,
p = 0.095).
The torsional stiffness of the four external fixator configurations was
determined to be similar (Kruskal-Wallis test, chi square = 1.76, 3 degrees of
freedom, p = 0.63). Pairwise comparison was only performed between the
external fixator with the lowest median (the semirigid system) and the tibial
nails (unreamed tibial nail and angle-stable nail) and between the tibial
nails. A significantly lower torsional stiffness was determined for the
unreamed tibial nail compared with the semirigid fixator (p = 0.004, a =
0.0176, Bonferroni corrected). While the torsional stiffness of the
angle-stable tibial nails tended to be larger than the unreamed tibial nails
(p = 0.065, a = 0.05, Bonferroni corrected), it was still significantly
less than that of the external fixation devices (p = 0.009, a = 0.025,
Bonferroni corrected).
Due to large variances within the groups, a significant difference was only
determined between the anteroposterior shear stiffness of the fixators with
the highest and lowest medians (i.e., the angle-stable tibial nail compared
with the unreamed tibial nail; p = 0.002, a = 0.0167, Bonferroni
corrected). In anteroposterior bending, the rigid fixator was not
significantly different from the semirigid fixator (p = 0.093, a = 0.05,
Bonferroni corrected), but it was significantly greater than the
anteromedially mounted fixator (p = 0.004, a = 0.0167, Bonferroni
corrected). A difference could not be identified between the semirigid fixator
and the remaining fixators (i.e., semirigid compared with the unreamed tibial
nail; p = 0.041, a = 0.025, Bonferroni corrected).
The mediolateral shear stiffness of the medially mounted external fixator
was significantly lower than that of the anteromedially mounted external
fixator (p = 0.009, a = 0.0167, Bonferroni corrected). In mediolateral
bending, no clear trend between the stiffness of external fixators and tibial
nails could be seen because of the relatively large variances within each
group (Fig. 4).
Torsional Moment and Stiffness of Healing Tibia
After nine weeks of healing, the involved limb in most animals reached 60%
to 70% of the maximal torsional moment and 85% to 95% of the torsional
stiffness of the contralateral limb (Table
II, Fig. 5). Only
the group treated with the unreamed tibial nail had much lower values (52.8%
and 74.8%, respectively). No difference was found between the medians of the
external fixator groups (Fig.
5) (Kruskal-Wallis test, chi square = 4.77, 3 degrees of freedom,
p = 0.19). Pairwise comparison was only performed between the external fixator
with the highest median (anteromedially mounted external fixator) and the
fixator with the lowest median (medially mounted external fixator) and the
tibial nails (unreamed tibial nail and angle-stable tibial nail). The median
torsional moment to failure of the anteromedially mounted external fixator
group was significantly larger than that of the unreamed tibial nail group (p
= 0.005, a = 0.0167, Bonferroni corrected) and the angle-stable tibial
nail group (p = 0.043, a = 0.05, Bonferroni corrected) but was not
significantly larger than that of the medially mounted external fixator group
(p = 0.035, a = 0.025, Bonferroni corrected).
Relationship Between Failure Moment and Fixation Stability
The relationship between the torsional moment to failure
(Mtorsion) and the axial compressive stiffness component
(Kaxial) was best described by an inverse quadratic polynomial
(expressed in the following equation and graphically represented by the dotted
curve in Figure 6).
Mtorsion=-3.73×10-05 Kaxial2+0.153 Kaxial-77.6
Because of the nature of the inverse quadratic relationship, the torsional
moment to failure is at a maximum when the derivative of the function in the
equation above is equal to zero, i.e., when
dMtorsion/dKaxial = 0. Solving this equation gives an
optimal axial compressive stiffness of 2050 N/mm, which is close to the axial
stiffness in compression of the anteromedially mounted external fixator
(Table I).
Plots of the anteroposterior stiffness and the mediolateral stiffness
against the moment to failure showed that the moment to failure tended to
decrease with decreasing shear fixation stiffness. The relationship between
the failure moment (Mtorsion) and the mediolateral shear component
of in vitro fixation stiffness (KM-L shear) appeared to be strongly
linear and was best described by the following equation (graphically
represented by the dotted line in Figure
6).
Mtorsion=0.108 KM-L shear+45.8
The torsional moment to failure also appeared to decrease with decreasing
bending stiffness and decreasing torsional stiffness; however, no clear
relationship could be formulated between these stiffness components and the
torsional moment to failure.
Examination of the interaction between the axial and shear components of
fixation stiffness (Fig. 7)
demonstrated that axial stiffness together with high shear stiffness provides
excellent healing (as occurred with the anteromedially mounted external
fixator). If the axial stiffness is either increased or decreased from the
moderate range, the strength and stiffness of the callus is reduced despite
only a marginal change in the shear fixation stiffness (as in the cases of the
rigid fixator, semirigid fixator, and angle-stable tibial nail). If in
addition the shear fixation stiffness is reduced, the callus will have a
substantially lower torsional failure moment (as occurred with the medially
mounted external fixator and with the unreamed tibial nail).
Since fixation stability influences the healing outcome of fractures
treated with osteosynthesis, it is important to define the boundaries of
stability for optimal healing. In the present study, the relationship between
the strength and stiffness of the healed tibia after nine weeks and the in
vitro fixation stiffness was investigated. In general, a poor healing outcome,
as quantified by the torsional moment to failure, was associated with low
fixation stability. Closer examination of the influence of the individual
components of in vitro fixation stiffness revealed that the moment to failure
of healed tibiae decreased with decreasing shear fixation stability. However,
the maximum moment to failure was determined for a fixator with moderate axial
fixation stability. Healing outcome worsened for higher and lower levels of
axial fixation stability. Therefore, optimizing the axial component of
fixation stability may be necessary for timely callus-healing.
The fixation stability determines the interfragmentary movements, and
different modes of interfragmentary movement are believed to influence
bone-healing differently. The influence of interfragmentary shear on healing
has long been subject to
controversy3,14-16.
Insufficient shear stability has been suggested to delay healing by disrupting
the blood supply15.
However, a recent study by Bishop et al. concluded that interfragmentary shear
is not necessarily detrimental to
healing16. This
would appear to suggest that healing may be disrupted by insufficient shear
stability, but it does not imply that some interfragmentary shear movement is
necessary in order to achieve timely healing. In this study, the torsional
failure moment of the tibia decreased proportionately with decreasing
anteroposterior and mediolateral shear stiffness. However, the relationship
between the axial compressive fixator stiffness and the torsional failure
moment was best approximated by an inverse quadratic polynomial. This
indicates that midrange values of axial stiffness are optimal for healing, and
they support the results of experimental studies that have shown that
fracture-healing is best stimulated by moderate levels of axial
interfragmentary
movement12,17.
In plotting the axial component against the resultant shear component of
stability (Fig. 7), boundaries
for optimal fixation stability in the sheep model that lead to timely healing
could be defined.
Surprisingly, the torsional stiffness component did not show a clear
relationship with the healing outcome. However, by comparing the healing with
the use of the unreamed tibial nail and the other fixators, a threshold for
the rotational stability required could be determined. Although fixation with
the unreamed tibial nail had a lower axial stability, it was still comparable
with that of the rigid and semirigid external fixators
(Fig. 3). However, the axial
torsional stiffness of the unreamed tibial nail group was less than that of
all of the other fixator constructs (Fig.
3), as was the moment to failure of the tibiae treated with the
unreamed tibial nail (Fig. 4).
This indicates that the torsional stability of the external fixators
(approximately 3.0 Nm/deg) was within the threshold required for good
healing.
In the present study, we determined that external fixation in sheep
provided the greatest axial stability and resistance to shear and torsion.
Treatment with a conventional unreamed tibial nail provided the least
stability to the fracture and resulted in the lowest mechanical strength of
the healed tibiae at nine weeks postoperatively. The stability of the unreamed
tibial nail was improved by replacing conventional locking screws with
angle-stable locking
screws27, which in
turn improved the failure moment.
In contrast to external fixation, tibial nailing disrupts the blood and
cell supply from the bone marrow, hinders the regeneration of vessels, and
blocks endosteal callus
growth26,28,
which might explain the lower failure moment determined for the unreamed
tibial nail group. However, the contribution of the endosteal callus to callus
strength is substantially less than periosteal callus because of its close
proximity to the neutral axis and its comparatively small
size23,26.
Therefore, impaired development of endosteal callus is not expected to
influence the moment to failure measured in this study, as was confirmed by
the comparable healing outcome in the angle-stable tibial nail and external
fixation groups.
The present study is the first, as far as we know, to characterize
completely the biomechanics of clinically relevant fixation devices in a
standardized, in vitro test setup and then correlate them with the healing
outcome in the same in vivo experimental model. While the test setup did not
enable the influence of individual stiffness components to be tested
independently, it was possible to draw conclusions on the nature of the
relationship for two of the components. However, it should not be interpreted
that only the axial and shear components determine the healing outcome. As
illustrated by the unreamed tibial nail group, a threshold exists for axial
torsion stiffness below which healing is delayed. The trends seen in this
study support a number of reports in the literature that have shown that the
healing of long-bone fractures is particularly sensitive to the axial
interfragmentary movement or the axial fixation
stability12,16.
Other limitations of this study are the methods used to quantify healing
outcome and the large variability reported. The failure moment at nine weeks
was used in this study to quantify the healing outcome. The selection of this
time-point can be critical for the results. Since a completely bridged callus
undergoing remodeling may have the same strength and stiffness as a callus
just bridged, it has been suggested that earlier rather than later time-points
may be ideal for identifying mechanical differences in
healing23. A large
variability was observed in particular for the results of the in vitro
stiffness testing. This is to be expected because of the interspecimen
variability of the specimens used in mechanical testing of the fixator-bone
construct.
Conclusions that are based on animal experiments require careful
interpretation before extrapolation to human
applications29. A
number of attributes of the sheep osteotomy model make it suitable for
studying the influence of mechanics on fracture-healing. First, the size and
shape of the tibia and the time needed for a fracture to heal in sheep are of
the same order of magnitude as those in humans. Second, despite obvious
differences (biped compared with quadruped), there are similarities in the
magnitude of the loads
experienced30 and
similar load profiles have been determined in the mid-diaphysis of long bones
of both sheep30 and
humans31. Since the
mechanical conditions in the callus are a product of limb-loading and fixation
stiffness, similar mechanical conditions can be expected in both sheep and
humans. Therefore, the components of stability determined to be important for
healing are also expected to be relevant for the treatment of similar
transverse fractures in the clinical situation.
Until now it has been generally unclear how stiff a construct should be and
how large the range of optimal stiffness is for fast and uneventful healing.
In this study, a clear relationship between the stability of fixation and the
mechanical strength of the healing tibia was seen. Furthermore, it was
possible to define boundaries (Fig.
7) for the axial and shear fixation stabilities that lead to
optimal bone-healing in sheep. Optimizing axial stability and limiting shear
instability appear to be important for creating conditions for timely
fracture-healing. ?
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