Abstract
Background: Reconstruction of large skeletal defects secondary to
osteomyelitis is a challenging problem. The purpose of this study was to
evaluate the outcome of the use of a vascularized fibular graft to treat such
defects in children.
Methods: Eight patients with a mean age of seven years and a
skeletal defect with a mean length of 11.8 cm (range, 6 to 17 cm) were treated
with a vascularized fibular graft. A staged protocol was used for the five
patients with an active infection at the time of presentation. The first
procedure consisted of radical débridement, and at the second stage a
free (seven patients) or pedicled (one patient) vascularized fibular graft was
used. The mean follow-up time was 5.7 years.
Results: Union of the graft occurred primarily in seven of the eight
patients, at a mean of 3.5 months, and after iliac crest bone-grafting in the
remaining patient. There was no recurrence of deep infection. Complications
developed in two patients. The mean time to full weight-bearing by the seven
patients with a lower-extremity reconstruction was 8.4 months, and all
patients were pain-free and able to walk without supportive devices.
Conclusions: A vascularized fibular graft is a viable option for the
management of large skeletal defects resulting from osteomyelitis in
children.
Level of Evidence: Therapeutic Level IV. See Instructions
to Authors for a complete description of levels of evidence.
While most cases of osteomyelitis in children can be treated with
antibiotic therapy alone, some children with neglected or late-presenting
chronic osteomyelitis require surgical débridement of necrotic bone or
abscesses. This may result in large skeletal defects, which create
considerable morbidity for the patient, threaten the viability of the involved
extremity, and present a challenging problem for the treating surgeon.
Conventional autogenous bone-grafting is preferably used for defects of
<6 cm, but it has limitations for the treatment of larger
defects1; the
time-period for graft incorporation is prolonged, and the quantity of
available autogenous graft is limited. Moreover, in large defects associated
with infection, scarring of the soft-tissue envelope compromises
revascularization of the graft.
Vascularized bone grafts, such as the vascularized fibular graft, retain
their intrinsic blood supply, hasten bone-healing and
hypertrophy2, and
have been widely used for reconstruction of large skeletal
defects3-14.
Large defects of an infectious etiology constitute a particularly challenging
subgroup, and their management in adults appears to result in a less favorable
outcome compared with that of management of uninfected
defects9-11.
However, to our knowledge, no one has reported on the outcome of vascularized
bone-grafting used to treat large defects associated with osteomyelitis in
children. Extrapolating outcome data from series of adult patients to children
is problematic because of factors such as the increased healing response in
children, the potential for damage of the growth plate by the infectious
process, and the increased technical difficulty of performing microvascular
anastomoses on smaller-diameter vessels.
In this study, we evaluated the use of a vascularized fibular graft to
reconstruct a large skeletal defect secondary to osteomyelitis in a cohort of
children. Our purpose was to assess the union rate of the graft and determine
whether limb salvage and infection control can be achieved.
We performed a retrospective review of the medical records of children who
had undergone a vascularized bone-graft procedure for reconstruction of a
long-bone defect secondary to osteomyelitis. Approval was obtained from the
institutional review boards of both participating institutions. To be included
in the study, the patient had to be a child (have open physes), have a history
of osteomyelitis documented by positive cultures and/or imaging findings, have
a large skeletal defect (=6 cm in length) of an extremity, and have been
managed with a free or pedicled vascularized bone graft.
Eight consecutive patients fulfilled the aforementioned criteria and were
included in the study. There were five boys and three girls with a mean age of
seven years (range, four to fifteen years) at the time of reconstruction.
Relevant data on each patient are summarized in the Appendix. Seven defects
(three femoral, three tibial, and one combined femoral and tibial defect)
involved the lower extremity, and one defect involved the ulna. The mean
length of the skeletal defects was 11.8 cm (range, 6 to 17 cm). Five patients
had a segmental defect (mean length, 12.9 cm), whereas in three patients
approximately 50% of the cortex remained in continuity. The defect was the
result of surgical débridement for the treatment of osteomyelitis in
all patients. The osteomyelitis was hematogenous in six patients,
posttraumatic (following an open facture) in one patient, and postoperative
(following allograft reconstruction of the proximal part of the femur for the
treatment of Ewing sarcoma) in one patient. Staphylococcus aureus was
the most common organism, identified in six of the eight cases.
Seven of the eight patients were initially treated elsewhere and then
referred to our institutions. On presentation, six patients had a limb-length
discrepancy ranging from 2.5 to 7 cm (mean, 5.8 cm) and two patients had
undergone lengthening of the femur prior to the vascularized bone-graft
procedure. Five patients had an active infection on presentation and were
treated with a two-stage protocol, whereas three patients had had no clinical
or laboratory signs of infection for a minimum of one year prior to the
grafting and were treated with a one-stage reconstruction. The median duration
of infection was 11.5 months (range, six weeks to twelve years). A mean of six
procedures (range, three to ten procedures) had been performed prior to the
vascularized bone-grafting procedures.
Management Protocol
All patients were managed with a consistent protocol that included
débridement of the recipient site and the vascularized bone-graft
transfer. If there were no clinical signs of infection (erythema, swelling, or
drainage) or laboratory signs of infection (an elevated erythrocyte
sedimentation rate, C-reactive protein level, or leukocyte count),
débridement and reconstruction with the vascularized bone graft were
performed at one stage. If there were signs of active infection, a two-stage
reconstruction was performed.
The first stage of the two-stage reconstruction consisted of radical
débridement to ensure removal of all foci of infection. An extensive
resection of all avascular and infected bone was performed back to bleeding
tissue. Scarred and avascular soft tissue was also resected. Bone,
soft-tissue, and fluid samples were sent for aerobic, anaerobic,
mycobacterial, and fungal cultures. The wound was copiously irrigated, and
antibiotic-impregnated polymethylmethacrylate beads or spacer was placed at
the defect site for dead-space management and local antibiotic delivery.
Particular attention was directed toward making the diameter of the spacer
greater than the usual diameter of the fibula, to ensure adequate room and
preclude compression of the pedicle of the future vascularized graft. The
patients were treated with systemic antibiotic therapy for six weeks followed
by oral antibiotics for four weeks, and they were monitored for evidence of
resolution of the infectious process. Before the vascularized bone-graft
transfer was performed, none of the patients had any clinical signs of
infection and all patients had a normal erythrocyte sedimentation rate,
C-reactive protein level, and leukocyte count.
The time-interval between the first and second stages ranged from six to
twelve weeks. During this interval, the skeletal defect was stabilized by a
cast or splint and the children were at home and were allowed to walk with
crutches without weight-bearing on the involved extremity. Before the grafting
was done, magnetic resonance angiography was performed at both the recipient
and the donor site to evaluate the vascular anatomy and rule out the presence
of a peroneal magna artery (an anatomic variation in which the peroneal artery
is the only artery perfusing the foot), which would preclude the use of a
vascularized bone graft.
The second stage consisted of bridging of the defect with the vascularized
bone graft. All procedures were performed with a consistent surgical technique
for graft
harvesting4,15
with use of an operating microscope for the microvascular anastomoses. A free
vascularized bone graft was harvested from the contralateral leg in seven
patients, whereas a pedicled vascularized bone graft from the ipsilateral leg
was used to achieve knee fusion in one patient. The graft was harvested as an
osseous flap in seven patients and as an osteocutaneous flap in one. The mean
graft length was 15.5 cm (range, 8 to 20 cm). In the lower extremity, the
fibular graft was inserted into the medullary canal of the tibia or femur.
Additional stability was provided by an external fixator in three patients, by
plate fixation in one, and by free screws in two; no implants were used in one
patient. Plate fixation was used to stabilize the graft in the one ulnar
defect. An end-to-end arterial anastomosis was performed in four of the seven
free transfers, an end-to-side anastomosis was performed in one, and an
interpositional vein graft was used for both the artery and the vein
anastomosis in two. At the donor site, the distal fibular osteotomy was done
approximately 6 cm proximal to the tibiofibular syndesmosis and distal
tibiofibular transfixation was performed with a single screw to minimize
valgus
deformity5,16-19.
In the one patient with an osteocutaneous flap, the skin component was used
for postoperative vascular monitoring of the graft.
The patients were followed clinically and radiographically at regular
intervals. The involved extremity was braced, and weight-bearing was
restricted not only until healing of the vascularized bone graft but also
until hypertrophy of the graft had occurred.
The mean duration of follow-up was 5.7 years (range, two to ten years). The
outcome variables for the purposes of this study included the union rate, the
time to healing of the vascularized bone graft, the rate of limb salvage, and
the infection rate. We also assessed the prevalence of complications, the time
to full weight-bearing, and the range of motion of the adjacent joints.
The early postoperative course was uneventful, with the exception of one
patient (Case 6; see Appendix) in whom an arterial thrombosis developed six
hours following the surgery; the patient underwent immediate exploration and
thrombectomy with salvage of the graft.
Union of the graft and reconstruction of the bone defect were achieved in
all eight patients (Figs.
1-A,1-B,1-C,1-D,1-E).
Primary union of the vascularized bone graft occurred in seven of the eight
patients, at a mean of 3.5 months (range, 1.5 to six months), as determined by
evidence of bridging of three of the four cortices on plain radiographs.
Overall, fifteen of the sixteen graft-host junction sites healed primarily.
There was one nonunion of the distal graft-host junction site in a patient
(Case 6) with a tibial defect. The nonunion was managed with autogenous iliac
crest bone-grafting, and healing was achieved three months later (Figs.
2-A,2-B,2-C,2-D).
No deep infection recurred. There was one superficial wound infection that
responded well to limited débridement and antibiotic therapy (Case 6).
One patient (Case 3) sustained a fracture of the healed graft with hardware
failure at nine months following the surgery; it was successfully treated with
repeat plate fixation. A valgus deformity of the ankle of the donor limb, with
breakage of the syndesmotic screw, developed in the same patient. This was
managed with fixation with a new syndesmotic screw and bone-grafting of the
tibiofibular syndesmosis, which achieved a synostosis. Overall, complications
developed in two of the eight patients.
The mean time to full weight-bearing following the seven lower-extremity
reconstructions was 8.4 months (range, three to seventeen months) overall and
5.4 months (range, three to seven months) in the five patients who did not
have any complications. Two patients with an uneventful postoperative course
underwent a subsequent procedure (lengthening of the involved lower extremity
or epiphysiodesis of the contralateral one) for management of a pre-existing
limb-length discrepancy. Details of the outcomes for each patient are
presented in the Appendix.
At the time of final follow-up, limb salvage and control of the infection
had been achieved in all patients. All seven patients with a lower-extremity
reconstruction were able to fully bear weight on the lower extremity, and none
was using any assistive device or brace. A limb-length discrepancy of =2.5
cm was present in four patients, who all used a shoe-lift. Two of these
patients, with discrepancies of 5 cm (Case 3) and 3.5 cm (Case 6) at the time
of the latest follow-up, were treated with epiphysiodesis of the contralateral
lower extremity and the discrepancy is expected to decrease. At the time of
the latest follow-up, no patient reported pain in the reconstructed extremity.
Four patients had a full range of motion of the adjacent joints. Three
patients had limitation of knee flexion (0° to 90°, 0° to 90°,
and 0° to 60°), and one patient lost ankle dorsiflexion; however,
these limitations had been present prior to the vascularized bone-graft
procedure.
The application of vascularized bone grafts for the management of both
large (>6-cm) defects and smaller ones with a poor soft-tissue
bed3-14
is widespread because the graft has unique anatomic and biologic properties.
The size and straight configuration of the fibular graft allow it to fit into
the medullary canal of the femur or tibia, match the size of the forearm
bones, and facilitate reconstruction of extensive defects up to 26
cm4,15.
The fibula has dual vascularity, derived from endosteal and periosteal
vessels20, which is
retained when successful microvascular anastomoses are performed between the
graft pedicle and the recipient-site vessels. As a result, the vascularized
bone graft bypasses the process of creeping substitution, which characterizes
healing of avascular grafts, and involves graft necrosis, resorption, and new
bone formation. The vascularized bone graft maintains to a greater degree its
mass and architecture, is biomechanically stronger than an avascular fibular
graft, and demonstrates enhanced healing potential and
hypertrophy2. In
addition, the vascularized bone graft provides an important source of
vascularity in scarred and avascular recipient sites.
A few studies in the literature have focused on the application of the free
vascularized bone graft for the management of defects of infectious etiology
in adult
patients21-27.
However, to our knowledge, no one has evaluated the outcome of free
vascularized bone-grafting for reconstruction of large long-bone defects
secondary to osteomyelitis in children.
Vascularized bone-grafting has been established in the literature as a
viable technique for children with a large skeletal defect secondary to
congenital pseudarthrosis of the
tibia16,17,19,28.
Weiland et al. reported healing of both ends of the vascularized bone graft in
eighteen of nineteen children; fourteen had primary healing, and four had
healing following
bone-grafting19.
Dormans et al. reported healing in eleven of twelve children (six with primary
healing and five with healing after
bone-grafting)16,
and Simonis et al. reported healing in nine of eleven children (seven with
primary healing and two with healing after
bone-grafting)17.
The successful application of a vascularized bone graft in the management
of congenital pseudarthrosis of the tibia has been attributed to the radical
débridement and to the vascularized nature of the graft, which allows
incorporation despite the presence of an avascular tissue
bed16,19.
In our opinion, the same factors were responsible for the successful outcomes
in our series. By providing the means for reconstruction of large bone defects
(up to 17 cm in our series), free tissue transfer allows radical
débridement and resection of all pathologic
tissue29, which is
a critical factor for the resolution of infection. In osteomyelitis, bacteria
grow in biofilms attached to the surface of bone or foreign
material30,31.
This protective mode of growth shields bacteria from antibiotics and host
defense mechanisms, leading to persistence of the
infection32. With
the vascularized bone-graft technique, the surgeon will not hesitate to excise
any questionable tissue because of concern about the resulting defect.
Moreover, with a vascularized bone graft there is the potential for healing
irrespective of the status of the soft-tissue bed, which is often compromised
in patients with osteomyelitis.
The present study is limited by its retrospective nature and the small
number of patients, which did not allow comparisons of subgroups based on the
anatomic location of the defect. The functional assessment was based on basic
criteria, such as walking ability, range of motion, and pain. Use of validated
instruments for the evaluation of the functional outcome would provide more
detailed information on the function of these patients. Finally, we did not
attempt to compare vascularized bone-grafting with alternative treatment
strategies, such as iliac crest bone-grafting, transfer of the ipsilateral
fibula, or the Ilizarov technique. Therefore, we cannot comment on whether
vascularized bone-grafting is the treatment of choice for the management of
large skeletal defects associated with osteomyelitis.
Iliac crest bone-grafting has been used to bridge skeletal defects
secondary to infection in children. Fowles et al. treated tibial defects (4 cm
on the average) with a posterior tibiofibular graft (eleven cases) or with an
ipsilateral fibular transfer
(six)33. Infection
recurred in four patients. Healing was achieved in all cases, but the authors
did not provide data on the number of subsequent procedures. Daoud and
Saighi-Bouaouina used iliac crest bone-grafting for the management of fourteen
segmental defects of the tibia, which averaged 23% of the tibial
diaphysis34. There
were five recurrences of infection, and the bone-grafting procedure was
successful in only six of the fourteen cases; seven tibiae required additional
procedures and supplemental bone-grafting. There was one nonunion, attributed
to the failure of the bone graft to fill the defect sufficiently.
It may not be possible to harvest enough iliac crest bone graft to fill a
large skeletal defect, whether it is segmental or partial. Donor site
complications have been well documented and include persistent pain, injury to
the lateral femoral cutaneous nerve, and hematoma
formation35-37.
The need for a large quantity of graft to fill an extensive defect may lead
the surgeon to be too aggressive and increase the complication
rate38. In three of
the eight patients in our series, the defect was not segmental and involved
approximately 50% of the cortex; therefore, conventional iliac crest
bone-grafting may have been possible. However, because of the lengths of these
partial defects (8, 11.5, and 13.5 cm), there was concern about whether a
sufficient quantity of iliac crest bone graft would be available as well as a
desire to provide structural support to the joint.
Transfer of the ipsilateral fibula into the area of a tibial defect has
been used successfully in children with osteomyelitis, but the tibia had to be
protected for eighteen months and lateral bowing of the tibia occurred in all
nine reported
cases39. Also, this
technique is applicable only for diaphyseal defects of the tibia and requires
an intact ipsilateral fibula. May et al. warned that, in this setting, moving
an intact ipsilateral fibula makes the limb more unstable and, if there is
delayed union or nonunion of the transferred bone, secondary procedures may be
more difficult38.
In contrast to the pedicle graft, the free vascularized bone graft overcomes
anatomic limitations and is applicable to all skeletal sites.
The Ilizarov technique is a viable reconstructive option for the management
of large skeletal defects and has been used successfully in children with a
tibial defect due to
osteomyelitis40.
Kucukkaya et al. reported healing in all of seven children in whom a tibial
defect (mean length, 7.4 cm) was treated with the Ilizarov
method40. The
fixator was applied approximately for one month for each centimeter of the
defect, and pin-track infection occurred in all children. Naudie et al.
reported on a group of seven children who had undergone lengthening of an
average of 10 cm to address growth arrest due to
infection41. The
mean duration of treatment was eight months, and complications included
pin-site infection in five patients, fracture after removal of the fixator in
two, malunion in one, joint contracture or stiffness in three, and
disseminated intravascular coagulation in one. All patients had pain
postoperatively, and one needed prolonged hospitalization for pain control.
Velazquez et al. reported thirty-eight major complications in forty children
treated with the Ilizarov technique, including transient nerve palsy in four
patients, compartment syndrome in two, reflex sympathetic dystrophy in one,
cellulitis in one, equinus deformity of the ankle in four, and a knee
extension contracture in
one42. The rate of
major complications was significantly higher (p < 0.002) in patients who
had had a longer duration of treatment. Similarly, Bell et al. found that the
greatest number of complications occurred in patients who had undergone
excessive
lengthening43. In
our series, the extensive size of the defects would have predisposed the
patients to the development of complications from prolonged application of the
Ilizarov device. The time for healing of the vascularized bone graft does not
depend on the size of the defect, and the vascularized bone-graft technique
avoids the use of the cumbersome apparatus and the need for the patient's
and/or parent's compliance with pin-track care.
However, the vascularized bone-graft procedure is technically demanding,
requires expertise in microsurgical techniques, and may be associated with
complications. In our series of eight patients, there was one graft
thrombosis, one nonunion, one fracture of the graft, one superficial
infection, and one valgus deformity at the ankle of the donor limb. Valgus
deformity of the donor ankle is a risk, especially when the distal part of the
fibula has been
harvested44. Use of
a syndesmotic screw alone has been proposed as an effective means of
stabilizing the lateral aspect of the ankle joint and avoiding valgus
deformity5,16,18.
However, it may not always be adequate, and creation of a tibiofibular
synostosis is an
alternative19.
This study highlights the potential for successful management of a large
post-osteomyelitic defect with a vascularized fibular graft in a child. All of
the patients in this series were managed with a consistent protocol, and all
grafting procedures were performed by a single surgeon (M.S.) who was
experienced in microvascular techniques; therefore, variations of surgical
technique and limitations related to a learning curve were minimized.
In conclusion, a vascularized fibular graft can be used to reconstruct a
large skeletal defect secondary to osteomyelitis in children, with control of
infection and salvage of the involved extremity. It appears to be a viable
solution for this complex problem.
Tables showing details on all patients are available with the electronic
versions of this article, on our web site at
(go to
the article citation and click on "Supplementary Material") and on
our quarterly CD-ROM (call our subscription department, at 781-449-9780, to
order the CD-ROM). ?
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