Original Article www.ijoonline.

com
DOI: 10.4103/0019-5413.69310

Extracorporeal irradiated tumor bone: A reconstruction

option in diaphyseal Ewing’s sarcomas
Ajay Puri, Ashish Gulia, MG Agarwal, NA Jambhekar1, S Laskar2

Abstract
Background: Limb salvage in extremity tumors is now established as an oncologically safe option without compromising long-
term survival. En bloc resection followed by extracorporeal radiation and reimplantation is a biological reconstruction option in
diaphyseal Ewing’s sarcomas. We analyzed the results of 12 cases of diaphyseal Ewing’s sarcomas treated using this modality.
Materials and Methods: Between March 2006 and March 2008, 12 patients with Ewing’s sarcoma underwent enbloc resection
and reconstruction, with reimplantation of the sterilized tumor bone, after extracorporeal irradiation. There were eight males
and four females, with a mean age of 14 years (range 2 to 22 years). The femur was the most common bone involved (n=8)
followed by the tibia and the humerus (two cases each). All these patients were non-metastatic at presentation and received
chemotherapy as per the existing hospital protocol. The mean length of the bone resected was 20 cm (range 11 to 25 cm). The
specimen was irradiated with 50 Gy prior to reimplantation and stabilized with the host bone, using suitable internal fixation.
Standard biplanar radiographs were assessed for evidence of union on the follow-up visits. The functional status was assessed
using the Musculoskeletal Tumor Society Scoring system at the time of the last follow up. The mean follow up duration was
29 months (range 12 to 57 months).
Results: Two patients (17%) had early infection with graft removal, hence are excluded from any analysis of union, however they
are included when analysing complications such as infection. Rest 10 cases were analyzed for bony union at the osteotomy sites.
Sixteen (84%) of the 19 osteotomy sites united primarily, without any intervention. Implant failure and non-union was seen at
three diaphyseal osteotomy sites. The average time for union of all osteotomy sites was 7.2 months (range 3 to 13 months).The
average time for union of the metaphyseal osteotomy sites was 5.9 months (range 3 to 12 months) and of diaphyseal osteotomy
sites was 8.3 months (range 4 to 13 months). The mean Musculoskeletal Tumor Society Score was 27 (range 19 to 30) with a
mean of 27. Nine of the ten patients with lower limb involvement were independent ambulators without additional aids. At the
time of the last review, six patients were free of disease and six patients had died from the disease. There were two recurrences
around the operative site. Both were associated with disseminated disease and in both the recurrences were in the soft tissue,
away from the irradiated graft.
Conclusion: Extracorporeal irradiation is a useful, convenient technique for limb salvage in diaphyseal Ewing’s sarcomas when
there is reasonable residual bone stock. It is oncologically safe and has good functional results. A radiation dose of 50 Gy for
sterilizing the bone ensures adequate tumor kill, while minimizing the deleterious effects on the biomechanical and biological
properties of the bone. The use of appropriate implants for adequate internal fixation and supplementary bone grafting at the index
surgery may help reduce the need for subsequent additional interventions to achieve union. The limitations of this procedure are
that it is not applicable in tumor bones that are structurally weak and in bones with pathological fractures.

Key words: Ewing’s sarcomas, extracorporeal irradiation, limb salvage

Introduction With the advent of effective chemotherapy the outcome

of localized Ewing’s sarcomas improved significantly. The

I
n an earlier era local treatment of non-metastatic advantages of surgery, compared to radiotherapy alone, for
Ewing’s sarcomas with surgery (generally amputation) or local control, have also been adequately demonstrated in
irradiation alone was ineffective, as the large majority of numerous studies, advocating a multidisciplinary approach
patients died within five years, with disseminated disease.1,2 to these lesions.3-5

Departments of Orthopedic Oncology, 1Pathology, and 2Radiation Oncology, Tata

Limb salvage in extremity tumors is now established as an
Memorial Hospital, Mumbai, India oncologically safe option, without compromising long-term
Address for correspondence: Dr. Ajay Puri, survival. Most bone tumors occur in the metaphyseal area
Associate Professor, Department of Orthopedic Oncology, Room No: 26,
Tata Memorial Hospital, E. Borges Road, Parel, Mumbai - 400 012, India.
of the bones and resection with a wide margin generally
E-mail: [email protected] involves sacrifice of the adjoining articular surface.

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 Puri, et al.: Ewing’s sarcoma: Extracorporeal radiation and reimplantation

Megaprosthesis provides an effective reconstruction option time taken for union, and the functional outcomes after
in a majority of these cases, with good functional results.6,7 reconstruction.
Tumors in the diaphysis are relatively uncommon and
in most of these it may be possible to achieve adequate Materials and Methods
margins without sacrificing the adjacent articular surfaces.
Although there are reports of diaphyseal prosthesis, this Between March 2006 and March 2008, 12 patients
intercalary gap can be reconstructed using other methods with Ewing’s sarcoma underwent enbloc resection and
too. Reconstruction using biological options like autografts, reconstruction with reimplantation of sterilized tumor bone
allografts, and bone transport have shown good functional after extracorporeal irradiation [Table 1]. These patients
results.8,9 were identified by a retrospective review of a prospectively
maintained database. The medical records, imaging,
In recent times, there has been a lot of interest in disease status, and functional status were reviewed. There
using the patient’s own tumor bone and reimplanting were eight males and four females with a mean age of
it after it has been sterilized. The described methods 14 years (range 2 to 22 years). The femur was the most
of sterilization have included the use of autoclaving, common bone involved (n=8) followed by tibia and
microwave, pasteurizing, liquid nitrogen, and radiotherapy humerus (two cases each).
(extracorporeal radiotherapy).10-14 The principle is the same;
the tumor-bearing bone is excised enbloc, all soft tissues The average duration of the symptoms was 3.5 months
and macroscopic tumor removed, and the remaining bone (range 2 to 12 months). A tissue diagnosis was obtained
sterilized by any of the above mentioned methods before preoperatively from all the patients. In case slides and
being reimplanted. We have been using extracorporeal blocks (n = 6) from prior intervention were available,
radiation and reimplantation for bony tumors since 2006, these were reviewed at our institute. If not, a biopsy
and have done this procedure in more than 45 patients. In (n = 6) was performed. In a large majority of the cases we
this article we analyze and present the results of 12 cases preferred a core needle biopsy to obtain the tissue. The
of diaphyseal Ewing’s sarcomas treated using this modality. biopsy results were discussed in a multidisciplinary meeting,
We observed the complications arising after reconstruction, which included a radiologist and a pathologist specializing in
Table 1: Clinical details of patients
Case Age Sex Bone RL Diaphyseal Metaphyseal Complications Follow-up MSTS Current status
(cms) union union (months) score
(months) (months)
1 9 M Tibia 17 7 7 None 15 28 Dead pulmonary
metastasis
2 19 M Femur 18 12 12 None 39 29 Local recurrence
(36 months) + dead
disseminated disease
3 22 F Femur 19 4 6 None 18 27 Dead disseminated
disease
4 16 F Femur 22 - - Infection 57 28 Alive — Independent
ambulation on nail cement
spacer
5 16 M Femur 25 - - Infection 44 19 Alive — Flail limb
6 10 M Humerus 12 10 5 Radial N Palsy, 12 24 Dead pulmonary
implant failure (6 metastasis
months), non Union
7 2 M Femur 11 6 3 None 36 30 Alive
8 19 M Humerus 21 13 6 Implant failure (10 36 28 Alive
months), non-union
9 14 F Femur 30 Bipolar 3 None 18 24 Local recurrence
prosthesis (13 months) + dead
disseminated disease
10 11 M Tibia 23 6 6 Plate exposed — 34 30 Alive
Flap cover
11 15 F Femur 25 6 6 None 18 28 Dead — Refused post op
chemotherapy pulmonary
metastasis
12 16 M Femur 24 11 6 Implant failure (7 22 26 Alive
months), non-union
MSTS: Musculoskeletal Tumor Society

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 Puri, et al.: Ewing’s sarcoma: Extracorporeal radiation and reimplantation

bone tumors. Prior to surgery all the 12 patients underwent specimen was realigned with the host bone and stabilized
a thorough oncological assessment to determine the extent with suitable extramedullary internal fixation. This included
of local disease and the presence of distant metastases. standard dynamic compression plates (n=3), reconstruction
Staging studies, including plain radiographs and MRI of plates (n=2), custom-made plates (n=5), and a locking
the limb, CT scans of the chest, and total body scintigraphy compression plate (n=1). In one case involving the proximal
were performed. All these patients were non-metastatic femur, a bipolar prosthesis was inserted at one end to
at presentation. All the patients received neoadjuvant articulate with the acetabulum and the distal osteotomy
(induction) and adjuvant (maintenance) chemotherapy as was stabilized with a locking compression plate [Figure 1].
per the existing hospital protocol.
The average surgical time for the procedure was seven hours
The MRI was used to define the extent of the lesion, the (range 6 to 8.5 hours). The average blood loss was 1050 ml
involvement of the soft tissues, relation to the neurovascular (range 300 ml to 2300 ml). None of the patients received
bundle, and the level of transection of the bone. The postoperative radiotherapy. The patients were allowed to
primary goal of surgery was complete excision of the tumor, mobilize after surgery with the use of an appropriate brace
with preservation of the limb. A 2 – 3 cm marrow margin as or cast. Postoperative range of motion of the adjacent
calculated on the T1 WI MRI image was considered as an joint was permitted according to the stability of the entire
adequate resection margin. The mean length of the bone construct. In cases of lower limb disease, guarded partial
resected was 20 cm (range 11 to 25 cms). weight bearing using walking assists, progressed to eventual
full weight bearing, once evidence of the bony union was
After tumor excision, a sample of the marrow was sent for seen on the radiographs. Standard biplanar radiographs
a frozen section from both residual ends of the host bone, were assessed. Bridging across three of four cortices in
to confirm clear margins. The resected specimen was then biplanar radiographs was considered evidence of the union.
transferred to a separate sterile trolley, away from the main
The patients were asked to follow up every three months
operative field to avoid any contamination of the operative
for the first two years and every six months, subsequently.
field. Under aseptic precautions all the soft tissue including
Besides screening for disease surveillance, biplanar
the periosteum was stripped from the bone after inking the
radiographs of the local part were assessed at each visit.
closest soft tissue margin. This inking of margins helped the
The functional status was assessed using the Musculoskeletal
pathologist report on the adequacy of resection in the final
Tumor Society Scoring system at the time of the last follow-
histopathology report, which otherwise would not have
up.15 The mean follow-up for all patients was 29 months
been possible.
(range 12 to 57 months). The mean follow-up duration
The bone specimen was lavaged with normal saline and
wrapped in Vancomycin-soaked mops. This was then
wrapped in sterile polyethylene surgical drapes in two
separate layers and placed in a sterile container, which
was sent for extracorporeal irradiation. The resected bone
segment enclosed in the sterile pack was irradiated to a
dose of 50 Gy / 1 fraction, prescribed to the midplane of
the specimen, using 6 MV photons or 60Cobalt γ rays with
parallel opposing portals. The mean treatment time for
delivery of 50 Gy was 28 minutes (range 24 to 36 minutes).
The average time for transfer of the graft from the operating
room to completion of the radiation therapy procedure and
return of the irradiated specimen to the operating room
was 55 minutes (range 45 to 75 minutes). After returning
to the operative room the excised bone was prepared
for reimplantation. The marrow contents were removed
by reaming and the bone specimen was lavaged with a
high speed pulsatile lavage system to remove the residual
marrow tissue. Bone cement was packed in the medullary Figure 1: (a) Anteroposterior radiograph showing proximal and
cavity of the radiated graft. Care was taken to ensure that diaphyseal femur Ewing’s sarcoma (case 9). (b) Extracorporeal
irradiation and reimplantation, with cemented bipolar prosthesis
the cement was just short of the osteotomy sites, so as not to inserted at the proximal end. Nine months follow up showing prosthesis
interfere with the bony apposition and eventual union. The in situ and distal osteotomy united

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 Puri, et al.: Ewing’s sarcoma: Extracorporeal radiation and reimplantation

for survivors was 38 months (range 22 to 57 months). The to the patient as a whole and three factors specific to
mean follow-up duration for non survivors was 20 months either the upper limb or lower limb. For the upper limb,
(range 12 to 39 months). positioning of the hand, manual dexterity, and lifting ability
were assessed, while for the lower limb use of supports for
Results ambulation, walking ability, and gait were assessed. For
each of the six factors, values of 0 to 5 were assigned based
All resection margins were free of tumor on histopathology, on the established criteria. The result was expressed as a
as evaluated on the intraoperative frozen specimens and sum total, with a maximum score of 30, and as a percentage
the final definitive histopathology. One patient had transient of the expected normal function for the patient. The
radial nerve palsy and eventually recovered, and one patient Musculoskeletal Tumor Society Score for patients evaluated
(case 10) had postoperative skin necrosis requiring a flap at their last follow-up ranged from 19 to 30 months with
cover. Two patients (17%) had infection (case 4,5). In one of a mean of 27 months. Nine of the 10 patients with lower
them the graft was removed immediately and non-biological limb involvement were independent ambulators, without
reconstruction was done, using a nail cement spacer. The additional aids.
infection subsided and the patient did not require any
additional procedures. In the other case repeated attempts At the time of the last review, six patients were free of the
to salvage the graft with lavage were unsuccessful. The graft disease and six patients had died from the disease. Patients
was eventually removed and the defect reconstructed using with disseminated disease at time of last follow up were
a nail cement spacer. The infection persisted, necessitating referred for best supportive care and final status of these
removal of the nail cement spacer too. Currently the patients was confirmed by telephonic contact. Mean follow
patient has a flail limb and ambulates on crutches. In both up of non survivors was 20 months. Of those who died, one
cases the organisms were MRSA resistant to vancomycin. patient refused post surgery maintenance chemotherapy
The infection rate was similar to that with the use of bank and succumbed to pulmonary metastasis. Her osteotomy
allografts, which was the other modality of reconstruction united at 7 months. Two others developed pulmonary
we used for diaphyseal defects. metastasis and three patients developed disseminated
disease (distant failure at multiple sites). There were two
Implant failure and non-union was seen in three cases at recurrences around the operative site. Both were associated
three diaphyseal osteotomy sites (Case no: 6,8,12). All with disseminated disease and in both, the recurrences
required open reduction and repeat internal fixation, with were in the soft tissue, away from the irradiated graft. No
thicker plates and bone grafting, which eventually united at recurrence occurred in the reimplanted bone.
10, 11, and 13 months after index surgery. Thus additional
procedures were required in six of 12 patients (50%). These Discussion
included open reduction and internal fixation with bone
grafting in three patients, wound lavage and graft removal in Reconstruction of long intercalary defects after tumor
two patients, and flap cover for skin necrosis in one patient. resection is a challenging proposition, especially in
immunocompromised patients receiving cytotoxic
After excluding two cases of infection where the graft was chemotherapy. Custom-made diaphyseal implants provide
removed, 10 cases were analyzed for bony union at the the advantage of immediate weight bearing and ambulation,
osteotomy sites. In one of these a bipolar prosthesis was but are expensive and issues regarding loosening, wear, and
inserted at one end. Thus 19 osteotomy sites were analyzed breakage remain. Biological reconstructions provide a cost-
for bony union in 10 patients. There were 10 diaphyseal efficient and more durable reconstruction option. The use
and nine metaphyseal sites. Sixteen (84%) of 19 osteotomy of strut autografts and allografts has been well-documented
sites united primarily without any intervention. The average in the reconstruction of these defects.9,16 The use of non-
time for union of all osteotomy sites was 7.2 months (range vascularized strut autografts is often limited by the length
3 to 13 months). The average time for union of metaphyseal of the long resection gaps. Strut allografts, although a
osteotomy sites was 5.9 months (range 3 to 12 months) and useful option, are limited by their availability, as very few
of the diaphyseal osteotomy sites was 8.3 months (range surgeons in our country have access to bone bank facilities.
4 to 13 months). Distraction osteogenesis, although described, requires the
lengthy use of external pins and has thus not found universal
The functional status was determined at the final follow-up application as the primary modality in patients undergoing
using the Musculoskeletal Tumor Society scoring system. treatment for malignant bone tumors.17
This was based on the analysis of three factors (pain,
functional activities, and emotional acceptance) pertinent Reimplanting the sterilized tumor bone offers yet another

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 Puri, et al.: Ewing’s sarcoma: Extracorporeal radiation and reimplantation

option for reconstructing these defects. This procedure has higher in the diaphysis than in the metaphysis.16,21-24 In a
a number of advantages, as it provides an anatomically series of extracorporeal irradiation autografting of the femur,
size-matched graft for biological reconstruction. It is non-union occurred in five of the 32 host-donor junctions
inexpensive and helps restore bone stock. The reimplanted (16%), and union occurred faster at the metaphyseal than
bone acts as a scaffold for creeping substitution and at the diaphyseal junction.25 Our experience has been
incorporation. This procedure obviates the need for a bone somewhat similar. We had non-union occur in three of the
bank and avoids the issues of allograft procurement and 19 host-donor junctions (16%). In our series the average
the risks associated with the use of allografts, such as, graft time for union of the metaphyseal osteotomy sites was 5.9
rejection and transmission of viral diseases. The limitations months as against 8.3 months at the diaphyseal osteotomy
of this procedure are: It is not applicable in tumor bones, sites. All three of our non-unions associated with implant
which are structurally weak, and in bones with pathological failure were at the diaphyseal osteotomy sites [Figure 2].
fractures. Various methods of sterilization have been
described. Autoclaving the bone has the disadvantage of These possibly occurred because of the use of improper
causing severe injury to bone proteins and the collagen implants.26 In two cases (cases 6 and 8) weak plates were
matrix leading to considerable damage to the biological used and in one case (case 12) a shorter than necessary
and biomechanical properties of the graft. Pasteurization locking compression plate was used, with an inadequate
has also been used successfully for sterilization of tumor hold, in the host bone. All three eventually united after open
bone, with good early results.12 Extracorporeal irradiation reduction and repeat internal fixation with bone grafting.
of autogenous tumor bone and its use for reimplantation We did not primarily bone graft any of the osteotomy sites
was first described in 1968, by Spira and Lubin.18 Since of the cases in this series.
then, there have been various authors who have advocated
different radiotherapy doses for sterilizing the bone. We Infection has been a major problem both in allografts and
used a dose of 50 Gy, delivered in a single fraction, for irradiated autografts.27 Infection rates for allografts vary
sterilization of the tumor-bearing bone, as advocated by from 6 to 17.6% and for irradiated autografts it ranges
certain authors.10,13,19 They suggested that higher doses from 0 to 12%.16,21,22,28,29 We had infection occur in two of
were not necessary for tumor sterilization. Higher doses our 12 cases (17%). We were unable to salvage the graft in
of radiation would increase the total treatment time and both, illustrating the disastrous consequences of infection in
also carry the additional risk of other possible detrimental these large reconstructions. Wrapping the resected bone in
effects such as reduction in strength, revascularization, and Vancomycin soaked mops is an attempt to try and reduce
osteoconductive properties, thereby increasing the time the infection rate in these cases.
for union and incorporation.20
Local recurrence has been rarely reported after extracorporeal
The rate of non-union in intercalary reconstructions with irradiation.29 We had two recurrences around the operative
allografts has been reported to be as high as 63% and is site. Both were associated with disseminated disease and in

a b c d
Figure 2: Anteroposterior radiograph of Humerus (a) showing Ewing’s sarcoma (case 8). (b) Postoperative radiograph after extracorporeal
irradiation and reimplantation. (c) Non-union and implant failure at proximal diaphyseal osteotomy occured at 10 months followup. (d) Refixation
with eventual union at 13 months follow-up radiograph at 30 months shows sound union

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 Puri, et al.: Ewing’s sarcoma: Extracorporeal radiation and reimplantation

both, the recurrences were in the soft tissue, away from the internal fixation and supplementary bone grafting at index
irradiated graft. No recurrence occurred in the reimplanted surgery may help reduce the need for subsequent additional
bone. We also histopathologically analyzed both the grafts intervention to achieve a union. It is a highly technical
that were removed because of infection for any residual procedure and the best result can be obtained in structured
tumor. There was no evidence of disease in the retrieved musculoskeletal oncology services.
specimens.
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Source of Support: Nil, Conflict of Interest: None.
25. Krieg AH, Davidson AW, Stalley PD. Intercalary femoral

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