AJR 2004; 182:963-970
© American Roentgen Ray Society
Imaging of Vascularized Fibula Autograft Placed Inside a Massive Allograft in Reconstruction of Lower Limb Bone Tumors
Marco Manfrini1,
Daniel Vanel1,2,
Massimiliano De Paolis1,
Cristina Malaguti1,
Marco Innocenti3,
Massimo Ceruso3,
Rodolfo Capanna3 and
Mario Mercuri1
1 Dipartimento di Oncologia Muscolo-Scheletrica, Istituto Ortopedico Rizzoli,
Via Pupilli 1, Bologna 40136, Italy.
2 Present address: Institut Gustave Roussy, Rue Camille Desmoulins, Villejuif
94800, France.
3 Centro Traumatologico Ortopedico, Via Largo Palagi 1, Firenze 50139,
Italy.
Received July 1, 2003;
accepted after revision October 3, 2003.
Address correspondence to M. Manfrini
(marco.manfrini{at}ior.it).
Abstract
OBJECTIVE. Bone allografts and vascularized fibula autografts were
combined (the fibula inside the massive allograft) for skeletal reconstruction
in a homogeneous group of patients. To verify the biologic behavior of the
grafts, we followed the series using conventional radiography and CT
analysis.
MATERIALS AND METHODS. Twenty-four patients with bone tumors had
intercalary segments of tibia or femur reconstructed and were followed up for
36–120 months. Sequential radiographs and CT scans were analyzed.
RESULTS. Three types of behavior were observed. In 13 patients, the
allograft maintained its architecture without fracture, although a regular
enlargement of the inlaid fibula led to progressive integration with the
allograft. A dense line on allograft endosteum was the first sign of bone
bridges heralding fusion of the two grafts. In eight patients, fracture or
nonunion of the allograft occurred, and the autograft reacted with rapid
appearance of dense hypertrophy that again induced bridges to the allograft.
In three patients, no changes in autograft size and density were followed by
fracture with no callus formation. This behavior was interpreted as
unsuccessful vascularization of the autograft.
CONCLUSION. Sequential radiography and CT analysis enabled us to
understand the changes in a combined graft offering an original way to
revascularize bone allografts.
Introduction
After local resection of bone tumors, massive bone allografts used for
reconstruction remain poorly vascularized and often resorb or break, whereas
vascularized autografts often are not of the right size or shape. A
combination of a vascularized fibula autograft placed inside a massive bone
allograft was used in a consecutive series of intercalary reconstructions of
the lower limb in patients with primary bone tumors. The authors followed up
all patients for more than 3 years by sequential radiography and CT to analyze
the radiologic patterns and correlate them with the biologic behavior of these
combined grafts.
Materials and Methods
Between 1989 and 1996, 36 patients had combined bone grafts for
reconstruction of intercalary skeletal gaps after resection for bone tumor of
the lower limb. The technique consisted of replacing the affected skeletal
segment by massive deep-frozen bone allograft (similar to the resected bones)
properly prepared to receive on its endosteal surface a free fibula autograft
always harvested from the contralateral leg. Extremities of the fibula were
fitted inside residual bone stumps, and peroneal vessels were anastomosed to
local vascular pedicles by microvascular sutures. Initially, the diaphyseal or
metadiaphyseal allografts were longitudinally opened through a large window.
In more recent cases, the window was reduced in length and width, and the
fibula autograft inserted as an intramedullary rod in variable sections of the
allograft bone. Twelve patients were excluded from the study: two underwent
amputation 1 year after surgery, one because of infection and the other for
local recurrence of an angiosarcoma; another presented with a local recurrent
osteosarcoma 2 years after surgery and underwent amputation; and nine were
lost to follow-up.
The 24 patients studied included 16 males and eight females with an average
age of 14 years (range, 4–30 years). Diagnosis consisted of 13
osteosarcomas (12 classic, one periosteal), six Ewing's sarcomas, three
adamantinomas, one malignant fibrous histiocytoma, and one low-grade
fibrosarcoma. The proximal tibia was involved in 10 patients, the tibial shaft
in eight, the distal tibia in two, and the femoral shaft in four. Eight of the
10 proximal tibia resections were performed through an intraepiphyseal
osteotomy in patients with open physes (Figs.
1A,1B,1C).
The mean length of the reconstructed segment was 15.5 cm (range, 8–26
cm). Internal fixation was defined as large in the seven patients in whom long
plates bridged the whole implant. In the remaining 17 patients, fixation was
considered small, with screws or short plates to secure the implant. Seventeen
patients received pre- and postoperative chemotherapy according to their
diagnoses. Postoperative recovery included cast immobilization for 30–60
days. Then all patients wore a protective weight-bearing brace for a variable
period (range, 3–38 months; average, 16 months; median, 17 months).
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Fig. 1A. —9-year-old girl with osteosarcoma of proximal tibia. Dotted
line on radiographs corresponds to level of CT scans. Preoperative
anteroposterior radiograph shows metaphyseal ossified tumor.
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Fig. 1B. —9-year-old girl with osteosarcoma of proximal tibia. Dotted
line on radiographs corresponds to level of CT scans. Preoperative coronal
T1-weighted MR image (TR/TE, 500/20) shows tumor close to epiphyseal plate,
but no abnormal signal is shown in epiphysis.
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Fig. 1C. —9-year-old girl with osteosarcoma of proximal tibia. Dotted
line on radiographs corresponds to level of CT scans. Radiograph of resected
segment shows resection level through epiphysis (arrow).
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At a mean follow-up of 7 years (range, 3–10 years), all patients were
alive, one with inoperable metastases and two after surgical removal of
pulmonary metastases. All patients had radiographic examinations every 6
months in the first 3 years and once a year thereafter. A total of 70 CT
examinations of the implant were performed in 23 patients (one was followed up
only on radiography): one examination in five patients, two successive
examinations in five patients, three examinations in four patients, and four
or more examinations in the remaining nine patients. CT studies were obtained
on the same units (Sytec or Hi-Speed, General Electric Medical Systems), with
the same acquisition parameters and bone and soft-tissue window settings.
A retrospective consensus review done by a surgeon and a radiologist
evaluated on CT the following radiologic parameters: for the fibula, size,
bone diameter, and thickness and density of the cortex; and for the allograft,
thickness and density of the implanted bone (measured on CT or radiography for
size and thickness, and evaluated visually for density). Only obvious changes
in density (visible without measurements) were considered significant.
Fractures of the fibula autograft and of the massive allograft and subsequent
reaction (bone resorption or callus formation) were recorded. Changes in
density in the allograft–fibula interface were evaluated and monitored.
Fusion at the extremities of the grafts with the host bone and between the two
grafts with bone bridges was evaluated. Spongiosis of the fibula cortex was
considered when the fibula cortex was thickened and trabeculate like
cancellous bone.
Results
Diameter of the fibula increased in 21 patients. In eight of these, the
increase was associated with thickening of the cortex and was always
associated with allograft fracture. In the first postoperative year, the
density of the fibula decreased in four patients, was stable in 18, and
increased in two. A delayed increase in density was visible in eight patients
(six times after a fracture, twice after transverse fusion of the two
grafts).
Thirteen fractures of the fibula and 12 fractures of the allograft were
visible, which led to eight cases of hypertrophic callus formation on the
fibula and eight on the allograft, respectively. Hypertrophy of the fibula
occurred rapidly, always in the first month after the fracture and then
progressed in the following months (Figs.
1F,
2A, and
2B). The fractured allograft
evolved with progressive marginal resorption and small peripheral
ossifications (Fig. 3D), or it
was entrapped in the callus produced by the fibula (Figs.
2F,2G,2H).
On CT, a dense line appeared on the endosteal surface of the allograft in 15
patients 12–18 months after surgery; in eight of these, it clearly
increased in size and thickness during follow-up. Evidence of transverse
fusion was found in all but three patients. Bridges between the two grafts
were visible on CT in 18 patients after 2 years: large areas of osseous fusion
were evident in 14 patients, although small multiple dense bridges were seen
in four. Three patients could not be evaluated for bony bridges because of
large synthesis and metallic artifacts on CT, but their grafts were considered
transversally fused on radiography. Three patients did not present any
transverse fusion. Thickening and trabeculation of the fibula cortex
(spongiosis), resembling cancellous bone, were observed in nine patients where
the fibula was inserted in a cylindric allograft or after the longitudinal
fusion through large bridges.
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Fig. 1F. —9-year-old girl with osteosarcoma of proximal tibia. Dotted
line on radiographs corresponds to level of CT scans. Anteroposterior
radiograph at 2 years of patient who had been walking without any support for
a few months shows fibula fusiform hypertrophy and previously unnoticed stress
fracture (arrow).
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Fig. 2A. —10-year-old boy with intercalary reconstruction of proximal
tibia because of osteosarcoma. Dotted line on radiographs corresponds to level
of axial CT scans. Anteroposterior radiograph at 1 year shows patient wearing
partial weight-bearing brace. Undisplaced fracture (arrows) of both
grafts appeared with minimal pain and swelling.
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Fig. 2B. —10-year-old boy with intercalary reconstruction of proximal
tibia because of osteosarcoma. Dotted line on radiographs corresponds to level
of axial CT scans. Anteroposterior radiograph obtained 1 month after A.
After treatment in long leg cast, intense callus formation in fibula fracture
(solid arrow) is seen, although fracture lines on allograft
(dotted arrow) with resorption of allograft margins
(arrowhead) are more evident.
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Fig. 3D. —14-year-old boy with intercalary reconstruction of proximal
tibia for fibrosarcoma. Dotted line on radiographs corresponds to level of CT
images. CT scan at 4 years (obtained 3 years after C) shows fracture
(arrow) of allograft, although small ossifications
(arrowhead) are seen on allograft surface. Inner portion of this
implant did not change before and after complete weight bearing. After
fracture, no rapid hypertrophy of fibula occurred. All these were considered
signs of failure of transplanted fibula vascularity.
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Fig. 2F. —10-year-old boy with intercalary reconstruction of proximal
tibia because of osteosarcoma. Dotted line on radiographs corresponds to level
of axial CT scans. CT scan at 2 years (obtained 9 months after fracture) shows
intense hypertrophy of fibula. Fibula fracture callus (arrow)
penetrates fractured allograft.
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Fig. 2G. —10-year-old boy with intercalary reconstruction of proximal
tibia because of osteosarcoma. Dotted line on radiographs corresponds to level
of axial CT scans. CT scan at 3 years shows further increase of fibula
diameter with entrapment of residual allograft (arrowhead) by
hypertrophic callus (arrow).
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Fig. 2H. —10-year-old boy with intercalary reconstruction of proximal
tibia because of osteosarcoma. Dotted line on radiographs corresponds to level
of axial CT scans. CT scan at 5 years shows remodeling of both grafts
concomitant to spongiosis of newly formed bone (arrow and
arrowhead). In this implant, weight rapidly shifted to fibula after
allograft fracture and resorption. Fibula fracture callus penetrated allograft
fragments, inducing intense remodeling of allogenic bone.
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Three distinct radiologic patterns were observed. If the massive allograft
fused to the host bone at the osteotomy and maintained its architecture
without fractures, a slow and regular enlargement of the fibula autograft,
without thickening of the cortex, led to a progressive integration into the
allograft. A dense line on the endosteal surface of the allograft, clearly
visualized on CT, suggested the induction of an internal layer of ossification
and was the first step of a series of bone bridges heralding fusion of the two
grafts. This pattern was observed in 13 patients (Fig.
4A,
4B,
4C,
4D,
4E,
4F,
4G,
4H).
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Fig. 4A. —12-year-old boy with intercalary reconstruction of proximal
tibia because of osteosarcoma. Dotted line on radiographs corresponds to level
of CT images. Postoperative anteroposterior radiograph shows fibula autograft
(solid arrow) and massive allograft (dotted arrow).
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Fig. 4B. —12-year-old boy with intercalary reconstruction of proximal
tibia because of osteosarcoma. Dotted line on radiographs corresponds to level
of CT images. Anteroposterior radiograph at 1 year shows patient wearing
partial weight-bearing brace. Decrease in cortex density of fibula and
complete fusion of osteotomies (arrows) are evident.
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Fig. 4C. —12-year-old boy with intercalary reconstruction of proximal
tibia because of osteosarcoma. Dotted line on radiographs corresponds to level
of CT images. Anteroposterior radiograph at 3 years in patient who had been
walking for 18 months with no support shows further remodeling of implant.
Transverse fusion of transplanted fibula to allograft is noted.
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Fig. 4D. —12-year-old boy with intercalary reconstruction of proximal
tibia because of osteosarcoma. Dotted line on radiographs corresponds to level
of CT images. Anteroposterior radiograph at 6 years shows displaced fracture
(arrow) (healed in cast) of distal portion of implant.
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Fig. 4E. —12-year-old boy with intercalary reconstruction of proximal
tibia because of osteosarcoma. CT scan at 3 months shows fibula autograft
(solid arrow) and massive allograft (dotted arrows).
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Fig. 4F. —12-year-old boy with intercalary reconstruction of proximal
tibia because of osteosarcoma. CT scan at 1 year shows fibula diameter is
increased, but not its cortical thickness; faint line of density on endosteal
surface of allograft (arrow) starts to be visible.
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Fig. 4G. —12-year-old boy with intercalary reconstruction of proximal
tibia because of osteosarcoma. CT scan at 3 years shows dense line on most of
endosteal surface of allograft (arrow). Medial transverse fusion is
shown between spongiotic fibula cortex and endosteal allogenic bone
(arrowhead).
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Fig. 4H. —12-year-old boy with intercalary reconstruction of proximal
tibia because of osteosarcoma. CT scan at 6 years shows allograft is denser on
all its surface. Fibula cortex is increased in both thickness and density.
Medial fusion is complete. In this implant weight remained mainly on
allograft.
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When a fracture or nonunion of the allograft occurred, the living
vascularized graft reacted to the increased load by rapidly producing a fast,
dense cortical hypertrophy that induced bony bridges to the residual
allograft. This pattern occurred in eight patients (Figs.
1A,
1B,
1C,
1D,
1E,
1F,
1G,
1H,
1I,
1J and
2A,
2B,
2C,
2D,
2E,
2F,
2G,
2H).
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Fig. 1D. —9-year-old girl with osteosarcoma of proximal tibia. Dotted
line on radiographs corresponds to level of CT scans. Postoperative
anteroposterior radiograph shows fibula autograft (solid arrow) and
massive allograft (dotted arrow).
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Fig. 1E. —9-year-old girl with osteosarcoma of proximal tibia. Dotted
line on radiographs corresponds to level of CT scans. Anteroposterior
radiograph at 1 year shows patient wearing partial weight-bearing brace.
Fibula cortex is thin and porotic. Arrows indicate osteotomy sites.
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Fig. 1G. —9-year-old girl with osteosarcoma of proximal tibia. Dotted
line on radiographs corresponds to level of CT scans. Anteroposterior
radiograph at 4 years; patient had returned to sports activities at school.
Bowing of fibula (arrow) is due to its growth, although tibia has
lost its proximal growth plate.
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Fig. 1H. —9-year-old girl with osteosarcoma of proximal tibia.
Postoperative CT scan at 2 months shows fibula inserted in allograft. Solid
arrow indicates fibula autograft; dotted arrow indicates massive
allograft.
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Fig. 1I. —9-year-old girl with osteosarcoma of proximal tibia. CT scan
at 2 years shows intense hypertrophy of fibula. Its cortex increased in both
thickness and density (arrow). Fracture lines (arrowhead) in
allograft are noticed.
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Fig. 1J. —9-year-old girl with osteosarcoma of proximal tibia. CT scan
at 4 years shows further hypertrophy of fibula diameter creating osseous
bridge (arrows) between thickened cortex of fibula and endosteal
surface of allograft. In this implant, weight was first on allograft but
shifted to fibula after allograft fracture.
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Fig. 2C. —10-year-old boy with intercalary reconstruction of proximal
tibia because of osteosarcoma. Dotted line on radiographs corresponds to level
of axial CT scans. Anteroposterior radiograph obtained 3 months after B
when patient had returned to protected walking in partial weight-bearing
brace. Whole fibula graft hypertrophied with remodeling of fracture callus.
Fracture line of allograft (arrow) is still evident with further
resorption of fracture margins (arrowhead).
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Fig. 2D. —10-year-old boy with intercalary reconstruction of proximal
tibia because of osteosarcoma. Dotted line on radiographs corresponds to level
of axial CT scans. Anteroposterior radiograph at 5 years, when patient had
been walking without any support for 3 years, shows striking hypertrophy of
fibula autograft brought to fusion to residual allograft
(arrows).
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Fig. 2E. —10-year-old boy with intercalary reconstruction of proximal
tibia because of osteosarcoma. Dotted line on radiographs corresponds to level
of axial CT scans. CT scan at 1 year shows fibula autograft (solid
arrow) and massive allograft (dotted arrow).
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When no significant changes in fibula size, shape, and density were
observed, and the fracture did not present any periosteal callus formation,
then, ostensibly, vascularization of the autograft had failed. This pattern
was seen in three patients (Fig.
3A,
3B,
3C,
3D).
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Fig. 3A. —14-year-old boy with intercalary reconstruction of proximal
tibia for fibrosarcoma. Dotted line on radiographs corresponds to level of CT
images. Postoperative anteroposterior radiograph shows fibula autograft
(solid arrow) and massive allograft (dotted arrow).
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Fig. 3B. —14-year-old boy with intercalary reconstruction of proximal
tibia for fibrosarcoma. Dotted line on radiographs corresponds to level of CT
images. Anteroposterior radiograph obtained at 4 years in patient who had been
walking without any support for 2 years shows no changes in density or
thickness of fibula cortex (solid arrow). Undisplaced fracture is
evident on medial cortex of allograft (dotted arrow). Remodeling of
proximal osteotomy progressed from epiphyseal plate for almost 2 cm into
combined graft (arrowheads).
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Fig. 3C. —14-year-old boy with intercalary reconstruction of proximal
tibia for fibrosarcoma. Dotted line on radiographs corresponds to level of CT
images. CT scan at 1 year shows fibula inserted in allograft. Solid arrow
indicates fibula autograft; dotted arrow indicates massive allograft.
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Discussion
A limb salvage approach is currently feasible in most primary bone tumors
of long bones. When surgical margins are wide, no difference is seen between
the long-term survival of patients with amputation and those with limb
reconstruction [1]. Massive
allografts (usually fresh deep-frozen cadaver bone allografts) can restore
size and shape similar to that of the resected bone. The drawback is that
allografts are devoid of vascular supply, and infection, nonunion, and late
fractures are a risk. Recent results, though, show a reduction in complication
rates
[2–4].
Bone formation (by creeping substitution) occurs at graft–host
junctions, and a long time is presumed to be necessary, even in younger
patients, before remodeling of a massive allograft that remains for many years
as a dead spacer [5].
Histologic evaluation of retrieved massive allografts confirmed the slow
creeping substitution not exceeding 2 cm at the allograft–host
osteotomy, or no more than 2–3 mm at the outer part of the graft where
the allograft cortex is covered by the host soft tissues
[6,
7]. An MRI sequential study of
allografts [8] revealed minimal
endosteal enhancement during the first 2 postoperative years, but no endosteal
revascularization of massive allografts has ever been shown.
Although the vascularized fibula autograft is never quite the right size or
shape to bear the patient's weight, it may hypertrophy under a mechanical
load. It has been used in a previously irradiated or infected tumor bed or in
upper limb reconstructions
[9–12],
but complications are frequent
[13–15].
Vascularized fibula and massive allografts were combined in this series
with the fibula autograft touching the endosteal surface of the allograft
[16,
17]. In three patients, the
vascularized graft failed. No radiologic changes in fibula patterns were
visible, and after some time, both the allograft and the fibula graft
fractured with no callus formation. In the other cases, the vascularized graft
presented dimensional and structural changes over a long period of time, as
expected of a living bone.
The radiologic follow-up showed changes related to load distribution on the
different components of the implant. When the load was mainly on the allograft
or on the allograft and large synthesis, the fibula exhibited regular
hypertrophy without cortical thickening. If the fibula was well protected from
mechanical stress by being fitted into a cylindric allograft, progressive
spongiosis of the fibula cortex was the rule. In the interim, a line of
ossification was seen on CT at the endosteal surface of the allograft and
represented the first step in the induction of bony bridges between the two
grafts. To our knowledge, such a sign has not been described.
When the load shifted mainly to the fibula autograft after nonunion or
fracture of the allograft, the cortex of the fibula rapidly reacted to the
increased load with fast and dense thickening. As the fibula hypertrophied,
osteogenic lines again became evident on the endosteal surface of the
allograft. We think the osteoblastic activity of the fibula, enhanced by load
and microfractures, may induce a similar activity on the endosteal border of
the allograft. Both behaviors represent the ability of a living transplanted
bone to adapt to mechanical stress. When unstable fractures occurred, a
hypertrophic cortical callus formation was often visible not only on the
fibula but also on and into the allograft fracture, suggesting a deep
revascularization of the allograft tissue.
In conclusion, we analyzed sequential radiography and CT of combined frozen
allograft and vascularized fibula autograft for reconstruction of defects
after tumor resection to monitor, evaluate, and understand the changes over
time. Imaging revealed the osteogenic activity on the endosteal border of the
allograft and the first signs of fusion of the two grafts. These data describe
an original way of revascularization of the allograft bone by the
intramedullary insertion of a living fibula autotransplant.
Acknowledgments
We thank Lorna Saint Ange and Alba Balladelli for editing the manuscript
and Cristina Ghinelli for graphics work.
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Abstract
Introduction
