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Copyright 1996 by The Journal of Bone and Joint Surgery, Incorporated
Residual Disease following Unplanned Excision
of a Soft-Tissue Sarcoma of an Extremity*
BY SABRENA NORIAf, AILEEN DAVIS, M.SC, B.SC, P.T.t, RITA KANDEL, M.D., F.R.C.P.(C)t,
JEROME LEVESQUE, M.D.f, BRIAN O'SULLIVAN, M.D., F.R.C.P.(C)t, JAY WUNDER, M.D., F.R.C.S.(C)t,
AND ROBERT BELL, M.D., F.R.C.S.(C)t, TORONTO, ONTARIO, CANADA
Investigation performed at the University Musculoskeletal Oncology Unit, Mount Sinai Hospital, and the University of Toronto, Toronto
ABSTRACT: Sixty-five patients who had been referred to our unit for additional management after an
unplanned excision of a soft-tissue sarcoma of an extremity at another institution were studied retrospectively to determine the prevalence of residual tumor
and to identify factors that predict which patients will
have a tumor following such an excision.
Unplanned excision was defined as excisional biopsy or unplanned resection of the lesion without benefit of preoperative imaging and without regard for the
necessity to resect the lesion with a margin of normal
tissue. In each patient, histological evaluation of the
specimen removed at the unplanned excision had demonstrated positive resection margins, but postoperative
physical examination on our unit revealed no gross
evidence of residual tumor and no tumor was identified
on cross-sectional imaging of the local site. Patients
who had evidence of residual disease on physical examination or on imaging were thought to have definite
evidence of sarcoma at the site of the operative wound
and were therefore excluded from the study.
After multidisciplinary consultation, all patients
had a repeat resection at our cancer center. Extensive pathological sampling of the specimen from this
second procedure was carried out, with sections obtained at mean intervals of 1.2 ± 0.7 centimeters.
Nodules initially thought to indicate disease were identified grossly in twenty-seven (42 per cent) of the sixtyfive patients, but histological evaluation confirmed the
presence of tumor in only sixteen (59 per cent). Histological evidence of sarcoma was identified in seven
additional patients in whom gross nodules were not
apparent in the specimen. Thus, sarcoma was identified in a total of twenty-three (35 per cent) of the
sixty-five patients.
The mean duration of follow-up was forty-six
months (range, twenty-four to eighty months; median,
*No benefits in any form have been received or will be received
from a commercial party related directly or indirectly to the subject
of this article. No funds were received in support of this study.
tUniversity Musculoskeletal Oncology Unit, Suite 476 (S. N.,
A. D., J. L., J. W., and R. B.), and Department of Pathology (R. K.),
Mount Sinai Hospital, 600 University Avenue, Toronto, Ontario
M5G 1X5, Canada.
^Department of Radiation Oncology, Princess Margaret Hospital, 600 Sherbourne Street, Toronto, Ontario M4X 1K9, Canada.
650
thirty-nine months). The margins of the second resection were positive in nine (39 per cent) of the twentythree patients who had residual sarcoma. Five (22 per
cent) of the twenty-three had a local recurrence. Four
of the five patients who had a local recurrence had
positive margins on repeat resection. This rate of local
recurrence (five of twenty-three patients) was significantly higher than that in the remainder of our patients
who had a soft-tissue sarcoma of an extremity (sixteen
[7 per cent] of 227) (p = 0.03).
There was no association between the detection of
sarcoma at the second procedure and the initial size or
grade of the tumor, the use of irradiation preoperatively, or the interval between the initial, unplanned
excision and referral to our cancer center. These data
indicate that it is not possible to predict which patients will have residual tumor at the site of the operative wound. Therefore, it is prudent to advise repeat
excision for all patients who have had an unplanned
excision of a soft-tissue sarcoma of an extremity. Unplanned excision complicates decision-making in the
treatment of this disease and should be avoided.
The local treatment of a soft-tissue sarcoma in an
extremity has progressed from radical operative intervention, including amputation, to the use of multidisciplinary treatment and a less extensive resection that
emphasizes the preservation of function of the limb
as well as control of the disease1-2-5-9. The availability of
cross-sectional imaging with computerized tomography
and magnetic resonance imaging has contributed to the
development of better limb-sparing procedures. These
imaging modalities provide the clinician with a more
accurate assessment of the extent of the lesion and its
relationship to the surrounding normal structures; such
assessment is critical to the planning of limb salvage for
patients who have a soft-tissue sarcoma.
A patient who has a soft-tissue mass of an extremity
may be seen initially by a surgeon who has little familiarity with the principles of modern operative treatment
of sarcoma. In this situation, the surgeon may proceed
with an excisional biopsy or an unplanned resection
of the lesion without benefit of preoperative imaging
and without regard for the necessity to resect the sarcoma with a margin of normal tissue. Giuliano and EilTHE JOURNAL OF BONE AND JOINT SURGERY
RESIDUAL DISEASE FOLLOWING UNPLANNED EXCIi ON OF A SOFT-TISSUE SARCOMA OF AN EXTREMITY
ber characterized these procedures as "unplanned total excisions." In the current report, we use the term
unplanned excision synonymously with the term unplanned resection, to include patients who have had
an excisional biopsy or an unplanned resection without
preoperative imaging and without regard for the necessity to resect the tumor with a margin of normal tissue.
Frequently, both the surgeon and the patient are surprised when a diagnosis of sarcoma is made, and the
patient may be referred to a cancer center for consideration of additional management at that time.
When the surgeon and radiation oncologist decide,
in consultation, what type of additional treatment (if
any) should be advised after an unplanned excision,
they are handicapped by insufficient data. It is often
difficult to assess accurately the initial pathological margins of the resection, and it is impossible to estimate the
extent of tumor that remains at the site of an unplanned
excision. When the residual tumor burden is small, it
might be safe to manage the patient with irradiation
alone. However, when there is a substantial burden of
residual sarcoma in the wound, additional wide (if possible) resection of the previous operative site should be
advised, possibly in conjunction with preoperative or
postoperative irradiation.
Approximately one-quarter of new patients who
are referred to our multidisciplinary soft-tissue sarcoma clinic have been sent for an opinion regarding
additional management after an unplanned excision.
Our protocol has been to advise most patients who have
been managed with excision of a sarcoma and who
probably have positive resection margins to have complete resection of the previous operative site, with
or without adjuvant irradiation. After resection, we
have carried out gross and histological evaluation of
the second specimen to determine what proportion of
patients have residual tumor and what factors might
predict which patients will have a tumor at the operative
site following an unplanned excision.
More than one-third of our patients have had residual tumor at the operative site, but it has been impossible to predict which patients would have this finding.
Our observations indicate that resection (or repeat resection) at a musculoskeletal tumor center should be
advised for patients who have had an unplanned excision of a soft-tissue sarcoma, and that the initial operation should be performed at a musculoskeletal tumor
center.
Materials and Methods
All patients who were entered into this study met
six criteria: (1) they were first seen clinically on our unit
between January 1986 and February 1993 after having
had a recent excision of a soft-tissue sarcoma of an
extremity, (2) the initial operative and pathology reports
and the initial pathological material indicated positive
resection margins at the time of the initial operation, (3)
VOL. 78-A, NO. 5, MAY 1996
651
the initial physical examination on our unit revealed
no evidence of a mass at the initial operative site, (4)
neither computerized tomography (before 1989) nor
magnetic resonance imaging of the initial operative site
revealed any evidence of a mass, (5) a second resection
was performed by one of us (R. B.), a surgical oncologist, and (6) histological assessment of the specimen
obtained at the repeat resection was performed by another of us (R. K.), a musculoskeletal pathologist.
Several of these criteria for inclusion require further
definition and explanation. Assessment of the margins
of the first resection (done at the referring hospital) was
carried out in a rigorous fashion. Personal discussions
were frequently held between the surgical oncologist
and the initial surgeon to clarify the operative report.
There was similar consultation between the consulting
and the initial pathologist. Whenever possible, histological slides of the material from the initial resection
margins were reviewed by the surgeon and pathologist
(if the orientation of the margins had been preserved
after the unplanned resection), and in all instances the
original material was reviewed to evaluate the histological diagnosis and grade. The final determination of a
positive resection margin was based on previously reported criteria2.
We excluded patients who had a mass that was palpable on physical examination or that was evident on
cross-sectional imaging. There is little question that patients who have had an extensive incisional biopsy or
partial removal of a tumor have residual disease and
need additional operative treatment. Our goal was to
restrict the study to patients who had been referred
after gross removal of the tumor with an excisional biopsy but who had a high risk of microscopic residual
sarcoma.
Patients who had an unplanned excision and had
negative histological margins also were not included
in the current study. Additional management after unplanned excision was based on the extent of the margins
that had been achieved. If it could be clearly documented that radical compartmental resection had been
accomplished, observation was advised. If the initial resection margins were found to be free of disease histologically but the resection could not be characterized
as radical, radiation was generally administered postoperatively. Since these patients were not treated operatively at our center, they are not included in this
analysis.
Between 1986 and 1993, 292 patients who had a
soft-tissue sarcoma of an extremity were managed on
our unit; 137 of them had been referred after an initial operation that had been performed elsewhere. Of
these 137 patients, sixty-eight were excluded from the
study: sixty-four had a mass that was palpable on physical examination or evident on magnetic resonance
imaging or computerized tomography, and insufficient
data had been recorded for the remaining four. One of
652
SABRENA NORIA ET AL.
us (R. K.), a musculoskeletal pathologist, then reviewed
the specimens and histological slides for the remaining
sixty-nine patients. To characterize the adequacy of sampling of the specimen taken at the repeat resection, the
longest dimension of the specimen was divided by the
number of sections obtained. This number represented
the mean distance between the samples obtained from
the tumor. Four patients had relatively incomplete sampling of the resection specimen, and these patients were
excluded. This left sixty-five patients for whom complete data were available.
Before the repeat resection, the cases of all sixtyfive patients were discussed at a multidisciplinary conference attended by personnel from the radiology,
pathology, medical, surgical, radiation oncology, and
allied-health departments. These consultants decided,
on the basis of the initial pathology and operative reports as well as the imaging studies performed after the
unplanned excision, whether adequate treatment would
necessitate irradiation as well as operative intervention
(combined treatment). If they were certain that irradiation would be necessary because of the anatomical constraints to a wide, curative local resection, they next
considered whether there would be a benefit from radiation therapy before the operation. Preoperative irradiation was recommended only if it was obvious that
combined treatment would be needed and that at least
one of three situations was applicable: (1) the location
and extent of the initial procedure would make it technically difficult to provide optimum irradiation after the
second excision; (2) dissection during the second operation would be along a major neurovascular bundle,
with the possibility of leaving microscopic tumor on
these critical structures; and (3) the surgeon expected
that remote tissue flaps or skin grafts would be necessary during the second procedure. Preoperative irradiation consisted of a total of twenty-five fractions in five
weeks, with two gray given daily.
When the patients had not received irradiation preoperatively, the operative specimen was evaluated to
determine whether there was any gross or histological
evidence of sarcoma and, if so, whether it was close
to the margins of the repeat resection. If there was residual disease within two centimeters of the margins,
postoperative irradiation with sixty to sixty-six gray in
two-gray fractions daily was generally recommended.
The principles used in the planning and delivery of radiation therapy have been described in greater detail
elsewhere9.
The primary objective of the current study was to
determine, by histological examination, whether there
was residual sarcoma in the specimen obtained at the
repeat resection. To ensure that the specimen was processed satisfactorily, the surgeon always examined the
specimen with the pathologist in the frozen-section
suite of the operating room. After orientation of the
specimen, the tissue was serially sectioned at approxi-
mately one-centimeter intervals and the number of sections was recorded. The previous operative site was
identified, and the scar tissue was palpated and visually
examined for evidence of nodules. Multiple blocks were
prepared from the region of the previous resection and
were evaluated by the pathologist.
The null hypothesis for this investigation was that
there would be no variable (or variables) associated
with the finding of residual sarcoma in the wound. For
the purpose of this study, information with regard to the
size of the initial sarcoma was obtained whenever possible from the pathology report of the referring institution. These data were available for forty-eight of the
sixty-five patients. When this information was not available, we reviewed cross-sectional images of the initial
lesion (available for only three patients) or, if there was
no other data source (fourteen patients), we ultimately
relied on the surgeon's and patient's best estimate of the
size. Slides of material taken at the original operation
were reviewed to determine the grade of the tumor
(high or low) and the histological subtype.
The statistical methods included descriptive statistics and univariate logistic regression analysis (SAS-PC
version 6.03; SAS Institute, Cary, North Carolina). The
regression analysis was used to determine whether
there was a significant relationship between the frequency of identification of sarcoma in the sample from
the repeat resection and the initial grade of the sarcoma,
the initial size of the tumor, the interval between the
initial resection and the consultation by our multidisciplinary unit, and the preoperative use of irradiation.
The margins of the repeat resection were evaluated
in the specimen obtained during that procedure, and the
patients were followed to determine how many had a
local recurrence. In order to compare these data with
those for our remaining patients who had a soft-tissue
sarcoma of an extremity, we subtracted the sixty-five
patients in the study group from the total cohort of 292
patients, leaving 227 patients for comparison with the
study group. The comparison group included 155 patients who had been managed only on our unit with
needle or incisional biopsy before the resection and
seventy-two patients who had had the initial operation
elsewhere before being referred to our unit for definitive management. These seventy-two patients had had
biopsies (ranging from needle biopsy to extensive attempts at excisional biopsy) before referral, but all had
palpable disease (or disease evident on cross-sectional
imaging) that indicated the extent of involvement by the
tumor. The four patients who were excluded from the
study because of inadequate sampling of the specimen
obtained at the repeat resection were included in the
comparison group.
Results
The mean age of the thirty-four men and thirtyone women was fifty-four years. Twenty-five (38 per
THE JOURNAL OF BONE AND JOINT SURGERY
RESIDUAL DISEASE FOLLOWING UNPLANNED EXCISION OF A SOFT-TISSUE SARCOMA OF AN EXTREMITY
cent) of the sixty-five patients had a malignant fibrous histiocytoma; eighteen (28 per cent), a liposarcoma; eight (12 per cent), a leiomyosarcoma; seven
(11 per cent), a malignant schwannoma; four (6 per
cent), a malignant hemangiopericytoma; and one (2
per cent) each, an epithelioid sarcoma, a soft-tissue
chondrosarcoma, and a primitive neuroectodermal tumor. Nine patients had a low-grade sarcoma and fiftysix, a high-grade sarcoma. The median interval between
the initial operation and the definitive procedure was
thirteen weeks. Twenty-nine patients received irradiation preoperatively and eleven received it postoperatively after the resection margins had been evaluated;
the remaining twenty-five patients received no radiation therapy.
Samples from the specimen obtained at the repeat resection were taken at intervals of 1.2 ± 0.7 centimeters (mean and standard deviation). Gross nodules
thought to be sarcoma were identified in the specimens
from twenty-seven patients (42 per cent); however, histological evaluation confirmed the presence of disease
in only sixteen. In the remaining eleven, only scar tissue was demonstrated. Residual sarcoma was identified on histological examination in seven additional
patients, for a total rate of twenty-three (35 per cent)
of the sixty-five patients. In nine of these twenty-three
patients, the sarcoma was identified at the margins
of the repeat resection. Additional resection was performed in three of these nine patients, and negative
margins were finally achieved. In the remaining six patients, additional resection was thought to be inadvisable as it would have necessitated amputation or a
major loss of function of the limb (for example, sacrifice
of the sciatic nerve).
At the time of follow-up, after a mean of forty-six
months (range, twenty-four to eighty months; median,
thirty-nine months), five patients had a local recurrence
and eleven had metastases. Four of the five local recurrences were in patients in whom the repeat resection
had had positive margins, and all were in patients who
had had detectable residual disease. Two patients who
had a local recurrence were managed with an amputation. The rate of local recurrence in the twenty-three
patients who had residual tumor (five [22 per cent] of
twenty-three) was significantly higher than that in the
comparison group (sixteen [7 per cent] of 227) (p = 0.03,
Fisher exact test).
Logistic regression analysis revealed that the likelihood of finding sarcoma at the previous operative site
was not associated with the size (p = 0.98) or grade (p =
0.38) of the sarcoma or with the interval between the
initial resection and referral to our unit (p = 0.66) (continuous data). It was also not associated with preoperative use of irradiation (p = 0.16) (dichotomous data).
This analysis failed to demonstrate any variable that
could be used to predict which patients were most
likely to have residual sarcoma at the operative site
VOL. 78-A, NO. 5, MAY 1996
653
following an unplanned excision of a soft-tissue sarcoma
of an extremity.
Discussion
In the current study, at least one-third of the patients
who had no detectable tumor on physical examination
or cross-sectional imaging after an unplanned excision
of a soft-tissue sarcoma of an extremity had residual
sarcoma on histological examination of the specimen
obtained at the repeat resection. All of our patients who
had positive margins following an unplanned excision
performed at another institution had a second resection,
ensuring limited selection bias. Possible sources of error
that might have resulted in underestimation of the prevalence of tumor include the adequacy of sampling of the
specimen obtained at the repeat resection and the limitations of histological identification of sarcoma in operative scars, especially after preoperative irradiation.
The adequacy of sampling of the specimens was
evaluated by determining the number of sites that were
evaluated within the specimen. Samples from the specimen were taken at intervals averaging 1.2 centimeters,
and the sampling was most extensive in the region of
the previous operative scar. Thus, although it is possible
that the proportion of patients who had residual disease
was underestimated because of limitations in the evaluation of the specimens, the sampling was extensive. The
analysis of the gross specimen immediately after the
resection by both the surgeon and the musculoskeletal
pathologist also helped to ensure that complete information regarding the previous operative treatment and
irradiation was available4.
Even if sampling is adequate, histological identification of sarcoma within an operative wound is not
always straightforward. Proliferation of fibrovascular
repair tissue in a scar can resemble the cellularity found
in a mesenchymal malignant lesion. This difficulty can
be increased when the site has been irradiated before the resection. We and other authors have found that
sarcoma treated with irradiation is often replaced by
reparative fibroblasts, which may demonstrate atypia6.
Cellular atypia in fibroblasts following irradiation might
result in the overestimation of residual sarcoma. At present, there is no technique, other than the assessment of
the specimen by an experienced musculoskeletal pathologist, that would be more effective for identifying
microscopic deposits of residual sarcoma at a postoperative site. We are therefore reasonably certain that
our estimate is accurate within the limits of current
techniques.
Considering the frequency with which soft-tissue
sarcomas are initially treated with excisional biopsy or
an unplanned local resection, the relatively poor documentation in the literature of the likelihood of finding
residual sarcoma at the site of the operative wound is
surprising. Giuliano and Eilber reported on ninety patients who had been referred after an excisional biopsy;
654
SABRENA NORIA ET AL.
all had been managed with Adriamycin (doxorubicin)
and radiation therapy before the repeat resection. Despite this intensive preoperative treatment, the authors
found gross evidence of residual sarcoma in about onehalf of the patients. The discrepancy between their findings and our lower estimates is probably due to our
exclusion of patients who had disease that was detectable on physical examination or cross-sectional imaging.
Of the 137 patients who were referred after an initial
procedure done elsewhere, sixty-eight were excluded
for that reason. Some of these patients may well have
been included in the study of Giuliano and Eilber.
Peabody et al. found that seventy-four (43 per
cent) of 172 consecutive patients referred to the same
surgical oncologist between 1975 and 1990 had had
a marginal excision before referral. Their data indicated that a subcutaneous tumor (originating superficial to the fascia of the limb) was more likely to be
associated with a previous excision than a deep lesion
(originating deep to the fascia of the limb). These authors found evidence of residual sarcoma in about 50
per cent of the patients who had been referred after a
marginal resection. It is difficult to compare the findings
of Peabody et al. with those in the current investigation because of differences between the two populations of patients. Only sixty-five (22 per cent) of our
292 patients were referred after marginal excision. This
probably can be credited to education about the treatment of sarcoma that had changed the treatment practices of the referring surgeons by the time that our study
began (in 1986). Peabody et al. did not state whether
cross-sectional imaging was used to identify residual
gross disease before repeat excision. As mentioned previously, evidence of residual gross disease was a criterion for exclusion in the current study and probably
accounts for the somewhat lower prevalence of residual disease in our patients (35 compared with approximately 50 per cent).
The ability to detect residual disease with crosssectional imaging methods was evaluated by Hudson
et al. These authors reported on twenty-one patients
who had been referred after an excisional biopsy of a
sarcoma. Of thirteen patients who had no palpable tumor, eleven had no evidence of disease on computerized tomography; however, a tumor was detected in
seven patients on reoperation. The remaining eight patients had a palpable lesion; it was shown to be tumor
on reoperation in seven, but computerized tomography
had failed to detect the residual palpable lesion in two
patients and had underestimated the extent of the lesion
in two others.
On the basis of the estimate that at least one-third
of patients who have had an unplanned excision of a
soft-tissue sarcoma have recognizable disease in the
wound despite negative findings on physical examination and magnetic resonance imaging, it is disappointing
that there was no significant association between the
factors that were evaluated (the size and grade of the
tumor, the interval between operations, and preoperative irradiation) and the presence of disease. We had
hoped that the results of this study would permit us to
stratify patients who are referred after an unplanned
resection with regard to the risk of residual disease, in
order to advise them better.
The high prevalence of positive margins on analysis of the specimen obtained at the repeat resection
is of concern. Positive margins were identified in nine
of our twenty-three patients who were recognized to
have residual sarcoma. This rate is much higher than
the usual rate of positive margins (less than 10 per
cent) at our institution9. These poor oncological results are due to the difficulty of resecting a pre-existing
operative field that is contaminated by sarcoma but
lacks a central mass that can provide visual and tactile
clues as to the extent of the disease. This situation is
particularly difficult when critical neurovascular structures have been exposed during the initial resection
of the gross tumor. Previous dissection of these structures eliminates the anatomical planes on which the
surgeon relies when performing a limb-salvage procedure and necessitates the dissection of the nerve or
vessel, or both, out of dense scar tissue that may be full
of microscopic sarcoma. Alternatively, the nerve or vessel would have to be sacrificed to remove scar tissue
that may contain no recognizable disease. The difficulty
of achieving adequate margins of resection after an unplanned excisional biopsy is reflected in the fact that our
twenty-three patients who had residual sarcoma had a
significantly higher risk (p = 0.03) of local recurrence
compared with our total population of patients who had
a soft-tissue sarcoma in an extremity.
In summary, our data provide no assistance to surgeons in deciding whether disease is present in a scar,
but they do re-emphasize the difficulty inherent in advising patients who have had an unplanned resection
of a soft-tissue sarcoma of an extremity. Our findings
should serve to remind the surgeon that all patients who
have a subfascial mass should have cross-sectional imaging of the local site as well as incisional or needle
biopsy before resection is attempted. Unplanned excision of a deep soft-tissue sarcoma of an extremity complicates additional treatment and should be avoided.
References
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VOL. 78-A, NO. 5, MAY 1996
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