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Clinical Orthopaedics and Related
Research®
ISSN 0009-921X
Volume 475
Number 2
Clin Orthop Relat Res (2017)
475:511-518
DOI 10.1007/s11999-016-5090-y
Are Biopsy Tracts a Concern for Seeding
and Local Recurrence in Sarcomas?
Irene Barrientos-Ruiz, Eduardo José
Ortiz-Cruz, José Serrano-Montilla,
Daniel Bernabeu-Taboada & Jose Juan
Pozo-Kreilinger
1 23
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CLINICAL RESEARCH
Are Biopsy Tracts a Concern for Seeding and Local Recurrence
in Sarcomas?
Irene Barrientos-Ruiz MD, Eduardo Jose
´Ortiz-Cruz MD, PhD, Jose
´Serrano-Montilla MD,
Daniel Bernabeu-Taboada MD, Jose Juan Pozo-Kreilinger MD
Received: 28 May 2016 / Accepted: 12 September 2016 / Published online: 21 September 2016
ÓThe Association of Bone and Joint Surgeons12016
Abstract
Background A biopsy is the final step in the diagnosis of
sarcomas. Complete resection of the biopsy tract tradi-
tionally has been recommended in musculoskeletal
oncology guidelines, as that tract is considered potentially
seeded with tumor cells. However, to our knowledge, the
frequency and implications of contamination of the biopsy
tract—specifically with respect to the likelihood of local
recurrence—and the factors that affect cell seeding are not
well described.
Questions/purposes We asked: (1) How often are biopsy
tracts contaminated with pathologically detectable tumor
cells at the time of tumor resection? (2) What factors, in
particular biopsy type (open versus percutaneous), are
associated with tumoral seeding? (3) Is biopsy tract con-
tamination associated with local recurrence?
Methods This is a retrospective study of a database with
patient data collected from a single center between 2000
and 2013. We treated 221 patients with sarcomas. A total
of 27 patients (12%) were excluded and 14 (6%) were lost
to followup. One hundred eighty patients finally were
included in the analysis who either had biopsies at our
center (112) or biopsies at outside institutions (68). Of
those performed at our center, 15 (13%) were open and 97
(87%) were percutaneous; of those at outside centers, those
numbers were 47 (69%) and 21 (31%) respectively. Med-
ian followup was 40 months (range, 24–152 months).
During the study period, we generally performed percuta-
neous biopsies as a standard practice for the diagnosis of
bone and soft tissue sarcomas and open biopsies were done
when the percutaneous procedure failed to provide a his-
tologic characterization. The mean age of the population
was 48 years (range, 7–87 years); 60% were male; 42% had
bone sarcomas. Nineteen patients had preoperative radio-
therapy and 56 had postoperative radiotherapy. Fifty-seven
patients received neoadjuvant chemotherapy and 73 had
Each author certifies that he or she has no commercial associations
(eg, consultancies, stock ownership, equity interest, patent/licensing
arrangements, etc) that might pose a conflict of interest in connection
with the submitted article.
All ICMJE Conflict of Interest Forms for authors and Clinical
Orthopaedics and Related Research
1
editors and board members are
on file with the publication and can be viewed on request.
Each author certifies that his or her institution has or waived for the
human protocol for this investigation and that all investigations were
conducted in conformity with ethical and confidentiality principles of
research.
This work was performed at the Musculoskeletal Tumor Unit,
Orthopaedics and Traumatology Department, at La Paz University
Hospital, Madrid, Spain.
Electronic supplementary material The online version of this
article (doi:10.1007/s11999-016-5090-y) contains supplementary
material, which is available to authorized users.
I. Barrientos-Ruiz (&), E. J. Ortiz-Cruz
Orthopaedic Oncologist Unit, La Paz University Hospital, Paseo
de la Castellana 261, Madrid, Spain
e-mail: irenebarrientosruiz@gmail.com
I. Barrientos-Ruiz, E. J. Ortiz-Cruz
MD Anderson International Hospital, Calle Arturo Soria 270,
Madrid, Spain
J. Serrano-Montilla
Orthopaedic Oncologist Unit, Rey Juan Carlos University
Hospital, Madrid, Spain
D. Bernabeu-Taboada
Musculoskeletal Radiology Unit, La Paz University Hospital,
Madrid, Spain
J. J. Pozo-Kreilinger
Musculoskeletal Pathology Unit, La Paz University Hospital,
Madrid, Spain
123
Clin Orthop Relat Res (2017) 475:511–518
DOI 10.1007/s11999-016-5090-y
Clinical Orthopaedic
s
and Related Research
®
A Publication of
The Association of Bone and Joint Surgeons®
Author's personal copy
adjuvant chemotherapy. We determined what proportion of
biopsy tracts were contaminated by pathologic analysis of
the biopsy tract specimen; during the period in question,
our routine practice was to excise the biopsy tract when-
ever possible at the time of the definitive resection. Using
the logistic regression test and Mantel-Haenszel test, we
compared open with percutaneous biopsies in terms of the
proportion of those that were contaminated at our site and
for outside referral biopsies separately, because we do not
assume the level of expertise was the same (our site is a
referral tumor center). We compared the local recurrence-
free survival between patients with and without contami-
nation and between open and percutaneous biopsies using
the Kaplan Meier test, again separating those performed at
our site from those referred for purposes of this analysis.
Results Twenty-one of 180 biopsy tracts were contam-
inated (12%). Twenty of 62 (32%) of the open biopsies
and one of 118 (0.8%) of the percutaneous core needle
biopsies had cell seeding (odds ratio [OR], 56; 95% CI,
7–428; p \0.001. One of 97 (1%) percutaneous biopsies
performed in our center, and none of the 21 (0%) per-
cutaneous biopsies performed in other centers had
contaminated biopsy tracts (p = 0.047). Two of 15 (13%)
open biopsies performed at our center and 18 of 41(38%)
open biopsies performed at other centers had contami-
nated biopsy tracts (OR, 4; 95% CI, 1–7; p = 0.001). Four
of 74 (5%) bone sarcomas and 18 of 106 (17%) soft tissue
sarcomas had biopsy tract contamination (OR, 3; 95% CI,
1–10; p = 0.023). The local recurrence-free survival was
longer for patients without contaminated tracts (mean,
107 months; 95% CI, 74–141 months) than for those with
biopsy tract seeding (mean, 11 months; 95% CI, 1–20
months; p \0.001).
Conclusions Open biopsies were associated with an
increased risk of tumoral seeding of the biopsy site, and
tumoral seeding was associated with an increased risk of
local recurrence. However, it is possible that other factors,
such as increased complexity of the tumor or a difficult
location, influenced the decision to obtain an open biopsy.
Even so, based on these results, we believe that higher risk
of local recurrence may be caused by an incomplete biopsy
tract resection. In our opinion, the percutaneous biopsy
with neoadjuvant or adjuvant therapy is the preferred
method of biopsy at our center.
Level of Evidence Level III, therapeutic study.
Introduction
It commonly is assumed in musculoskeletal oncology
[3,5,14] that the biopsy tract must be resected together with
the tumor in limb-sparing surgery for sarcomas. Some authors
have recommended contamination of a biopsy tract as an
indication for amputation when the biopsy tract is impossible
to include in the surgical approach, affects the neurovascular
bundle, or wide margins are not possible [14,15]. Oncologic
surgeons now use different types of biopsies, which create
different kinds of biopsy tracts. The scar from a percutaneous
core needle biopsy is a puncture of the surface, but in deep
tissues it has a tridimensional shape that is difficult to predict
reliably. The accuracy of core needle biopsies ranges from
77% to 97% in published series [16,17,22,28–34]. It is
excellent for bone sarcomas (77%–96%) and possibly less so
for soft tissue sarcomas (76%–78%). However, the sensitivity
in soft tissue sarcomas improves with image-guided core
needle biopsy (special contrast-enhanced ultrasound) and
with a pathologist with extensive experience working with
limited samples [7,17,19]. The accuracy of open biopsies is
close to 100% in some reported series [1,17,21], but the cost
and the possibility of complications are higher [1,2,17,21].
They are used more commonly in centers without experi-
enced sarcoma experts [1,2,17]. An open biopsy produces a
longitudinal scar that may be variable in morphologic fea-
tures and direction.
Some authors have suggested that complete resection of
the percutaneous biopsy tract rarely is achieved [10].
Although resection of the biopsy tract is recommended by
numerous authors [5,13,14], neither we nor Oliveira et al.
[20] could find a study that definitively confirmed the fre-
quency of biopsy tract seeding or that there is increased risk
of local recurrence when the biopsy tract is not resected.
We performed a pathologic analysis of the muscu-
loskeletal sarcoma biopsy tracts of patients treated at our
institution during 2000 to 2013. The main objective was to
identify factors associated with contamination. We define
‘‘contaminated biopsy tracts’’ or ‘‘biopsy tract seeding’’ as
those in which the pathologists actually find tumor (viable
or necrotic) cell nests anywhere in the resected biopsy tract
of the main tumor at the time of definitive resection. The
secondary objective was to detect the relevance of tumor
seeding in local recurrence-free survival of the series. We
asked the following questions: (1) How often are biopsy
tracts contaminated with pathologically detectable tumor
cells at the time of tumor resection? (2) What factors, in
particular biopsy type (open versus percutaneous), are
associated with tumoral seeding? (3) Is biopsy tract con-
tamination associated with local recurrence?
Patients and Methods
After institutional ethical board approval, we performed a
study in which we included 221 patients with bone and soft
tissue sarcomas treated at our tertiary referral
512 Barrientos-Ruiz et al. Clinical Orthopaedics and Related Research
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musculoskeletal oncology center from March 2000 until
March 2013. This is a retrospective observational study of
prospectively collected data of the medical records, surgi-
cal protocols, radiologic studies, and pathologist reports.
Forty-one of the 221 patients were excluded; 14 were lost
to followup and therefore not included for analysis. The
samples of four patients were ulcerated or infected and
therefore these four patients were not eligible for inclusion
in the study. Twenty-three biopsy tracts were not resected
because either the biopsy was performed at another hos-
pital and we were not able to find the scar, or the scar
resection would have led to an ablative surgery and the
patient rejected amputation. Apart from these cases just
mentioned, during this period, our practice was to excise
and histologically examine the biopsy tract at the time of
definitive resection of the sarcoma. We included all the
patients with a diagnosed musculoskeletal sarcoma who
had their final surgery at our hospital even if the biopsy had
been performed elsewhere before the referral (Table 1).
Median followup was 40 months (range, 24–152 months).
During this study period, of the biopsies performed at
our center and included in this series, 15 of 112 (13%) were
open and 97 of 112 (87 %) were percutaneous; of those at
outside centers, those numbers were 47 of 68 (69%) and 21
of 68 (31%), respectively. During the study period, we
generally performed percutaneous biopsies as a standard
practice for the diagnosis of bone and soft tissue sarcomas
and open biopsies when the percutaneous procedure failed
to provide a histologic characterization. We compared
open with percutaneous biopsies, in terms of the proportion
of those that were contaminated, for our institution and for
outside referral biopsies separately, as we do not assume
the level of expertise was the same (our institution is a
referral tumor center). We compared local recurrence-free
survival between patients with and without contamination
and between open and percutaneous biopsies, again sepa-
rating those performed at our institution from those
referred, for purposes of this analysis.
If the patient was referred from another center, our
pathology team reviewed the samples to determine if a new
biopsy was needed. We routinely performed core needle
biopsies as standard procedure for histologic diagnosis of
bone and soft tissue tumors. Two senior musculoskeletal
radiologists performed all the biopsies (DB-T, MTV). Bone
biopsies were performed in most cases using CT guidance,
but also targeted to the periphery of the tumor. In some
cases with cortical breakout, ultrasound guidance was used.
Bone biopsy was performed using a T-Lok
TM
ultrasound-
guided (Argon Medical Devices, Plano, TX, USA) or a
Bonopty
TM
(AprioMed, Uppsala, Sweden) coaxial needle.
For soft tissue malignancies biopsy, we use ultrasound
Doppler color guidance targeted to the most vascularized
area and in some cases we also use contrast-enhanced
ultrasound. In a soft tissue sarcoma, this area usually cor-
responds to the periphery of the tumor. The majority of soft
tissue biopsies were performed using a coaxial technique,
that is, by inserting an introducer or sheath to the edge of
the lesion or just inside the lesion and then advancing a
cutting needle through the introducer or sheath into the
lesion to obtain the biopsy samples. From 2000 to 2010 a
Table 1. Baseline epidemiologic population characteristics
Characteristic Totals
Age of patients (years) Median, 48.17 (range, 7–87
years)
Gender 106 males (60%); 74 females
(40%)
Location of tumor
Upper limbs 20%
Lower limbs 70%
Extracompartmental 8%
Axial skeleton 2%
Laterality
Right 52%
Left 47%
Axial 2%
Bone sarcomas 42%
Soft tissue sarcomas 58%
Biopsies performed at authors’
institution
62%
Biopsies done at other centers 38%
Biopsies done at both 3%
Percutaneous biopsy 66%
Open biopsy 26%
Both 9%
Diagnosis
Chondrosarcoma 15%
Leiomyosarcoma 8%
Liposarcoma 14%
Osteosarcoma 19%
Others 15%
Primitive neuroectodermal tumor/
Ewing
4%
Pleomorphic sarcoma 16%
Synovial sarcoma 14%
Grade
19%
21%
3 66%
44%
Margins
Marginal resection 19%
Wide resection 79%
Other 2%
Volume 475, Number 2, February 2017 Biopsy Seeding and Relevance in Practice 513
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TruCore-II
TM
(Argon Medical Devices) was used; since
2010 we use the Speedybell coaxial biopsy system (Biop-
sybell Srl, Mirandola, Italy) to infiltrate the periosteal
layer.
Needle size depends on the difficulty in obtaining a
representative tumor sample (myxoid, heterogeneous
tumors, or necrotic tumors), but usually a 16-gauge needle
is used to get thick cylinders of tumor and only two or three
passes are made. Samples usually were placed in a 10%
formalin solution and hand-delivered to the pathology unit
for analysis. However, each case is reviewed during weekly
meetings before the biopsy to determine the number of
samples, the approach [12], and the delivery (fresh or
formalin). At our center, the same oncologic orthopaedic
team performing surgery on the patient also performs all
the open biopsies when they are needed. The patients who
are referred are discussed during a weekly meeting [9,27];
if the open biopsy was performed in line with the predicted
incision and the surgeon was aware of the possible neo-
plastic nature of the lesion, the biopsy was considered to
have been correctly performed. If the open biopsy is not
considered appropriate (ie, not performed correctly) and
limb-sparing surgery is still possible, we plan a wider soft
tissue resection (often together with plastic surgery).
Nineteen patients had preoperative radiotherapy and 56
had postoperative radiotherapy. We considered preopera-
tive radiotherapy as a possible bias in the adjusted analysis
because some authors [4] point to radiotherapy and
chemotherapy as being probable influences to biopsy tract
contamination. They did not resect the core needle biopsy
in 59 patients with neoadjuvant therapies.
The biopsy tract was resected together with the tumor
following the standard of treatment for a wide oncologic
resection. We could identify the scar of the percutaneous
biopsy tract because it was labeled with India ink in the
dermis. In the final surgery, we use the images (ultrasound,
CT-guided biopsies) if they are available and manual pal-
pation to include the deep tract as completely as possible.
The margins of the main tumor resection were evaluated.
We consider the margins wide when the distance between
the closest border and the pseudocapsule is wider than 1 cm
or 2 mm with anatomic barriers (periosteal layer, epi-
neurium, fascia, or vessel adventitia). The sample is sent to
the same pathologists (FLB, JJPK) and reviewed inde-
pendently macro- and microscopically (Fig. 1). The
technique used in pathologic analysis consists of cutting 2-
mm parallel blocks of all tissue surrounding the macro-
scopic scar and the 2-mm blocks were cut in 4-lthick
sections, stained with hematoxylin and eosin, and the
pathologist specifically searched for a tumoral cell nest in
the sample. Immunohistochemical tests were used if nec-
essary for histologic characterization. The tumor stage is
recorded according to the American Joint Committee on
Cancer 2010 and Enneking classification for bone sarcomas
[8]. The patients were evaluated with MRI and CT every 3
months for 2 years, then every 6 months until 5 years, and
finally annually. Bone sarcomas with prosthesis recon-
struction also are evaluated with a bone scan and
ultrasonography every 6 months. Median followup was 40
months (range, 24–152 months).
Descriptive statistics were analyzed. The statistical
analysis was performed using SPSS software, Version 16.0
(SPSS, Chicago, IL, USA). We used a univariate chi-
square test for each variable. We analyzed separately, with
the Mantel-Haenszel test, contamination of the open and
percutaneous biopsies performed at our center and those
performed in other hospitals. We performed a multivariable
analysis using the logistic regression proportional model to
detect the factors that can affect biopsy tract contamina-
tion. We also compared the local recurrence-free survival
in patients with and without biopsy tract seeding using the
Kaplan-Meier method using the log-rank test. Statistical
significance was accepted as a probability less than 0.05.
Results
Twenty-one of the 180 samples (12%) were contaminated,
with macroscopically detectable cell nests in two and
microscopically detectable cell nests in 19. One of the 21
contaminated biopsy tracts was from a percutaneous biopsy
(0.8% contamination rate). One of 97 (1%) percutaneous
biopsies performed at our center and none of the 21 (0%)
percutaneous biopsies performed at other centers had
tumoral cell seeding (p = 0.047). This one patient with a
contaminated needle biopsy had a Grade 1 chondrosarcoma
and underwent extended intralesional resection with high-
Fig. 1 This microscopic image of a biopsy tract shows an osteosarcoma
cell nest (Stain, hematoxylin & eosin; original magnification, 910).
514 Barrientos-Ruiz et al. Clinical Orthopaedics and Related Research
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speed burring and phenol. The biopsy was performed to
confirm that this patient had a low-grade, rather than high-
grade, chondrosarcoma. The patient has 4 years of fol-
lowup and no evidence of disease. The other 20 of 21
contaminated biopsy tracts were from open biopsies (32%)
(mean, 55 months; 95% CI, (7–428 months; p \0.001).
Open biopsies were more likely to be contaminated than
percutaneous biopsies, among the patients whose biopsies
we performed and those whose biopsies were performed at
referral centers. Two of 15 (13%) open biopsies performed
at our center and 18 of 41(38%) open biopsies performed at
other centers had contaminated biopsy tracts (p = 0.001;
odds ratio [OR], 4; 95% CI, 1–7). Other factors associated
with an increased risk of biopsy tract contamination were
soft tissue sarcoma and biopsies performed at other centers
before the patient was referred to us (Appendix 1. Sup-
plemental material is available with the online version of
CORR
1
.) Four of 74 (5%) bone sarcomas and 18 of 106
(17%) soft tissue sarcomas had biopsy tract contamination
(OR, 3; 95% CI, 1–10; p = 0.023). We could not find
differences in the following variables: age, sex, location,
grade, stage, neoadjuvant chemotherapy, number of per-
cutaneous core needle biopsies, tumor resection margins,
or time from the biopsy until definitive surgery. None of
the patients with preoperative radiotherapy had a contam-
inated biopsy tract. The center where the biopsy initially
was performed was not a factor for biopsy tract contami-
nation in the multivariable analysis. However, the bone or
soft tissue sarcoma and the type of biopsy are independent
factors (Table 2).
The local recurrence-free survival was longer for
patients without contaminated tracts (mean, 107 months;
95% CI, 74–141 months) than in those with biopsy tract
seeding (mean, 11 months; 95% CI, 1–20 months; p \
0.001) (Fig. 2). The local recurrence-free survival did not
show statistical differences between patients with
percutaneous and open biopsies, neither at our center nor in
patients whose biopsies were performed at another hospi-
tal. With the numbers we had, we could not show a
difference in local recurrence-free survival in percutaneous
biopsies (mean, 102 months; SD, 12 months; 95% CI, 77–
127 months) compared with open biopsies (mean, 98
months; SD, 10 months; 95% CI, 80–117 months; p =
0.252) (Fig. 3). We also did not observe a difference in
local recurrence-free survival between patients who had
their biopsy at our hospital or at other hospitals.
Discussion
The biopsy is a key step in the diagnosis of sarcomas as
incorrectly performed biopsies might result in more abla-
tive final operations or might compromise the oncologic
resection [14,15]. Guidelines recommend biopsy tract
resection in the definitive surgery to achieve complete
elimination of malignant cells [5,13,14]. To our knowl-
edge, and as reported by Oliveira et al. [20], contamination
of the tract and the factors that can affect seeding have not
been reported. We detected contamination with tumoral
cells in 12% of the biopsy tracts. Tumoral cell seeding
increased in open biopsies performed at referral centers or
at our center. The local recurrence-free survival was longer
in patients without contamination of the biopsy tract.
There are limitations in this study. First, the retrospec-
tive design may have resulted in some selection bias in
terms of which patients received open biopsies and which
Table 2. Logistic regression proportional multivariable analysis
Variable Odds ratio
(95% CI)
p Value
Open biopsies
Percutaneous biopsies
51,047 (5389–
483,506)
\0.001
Bone sarcomas
Soft tissue sarcomas
5907 (1659–
21,035)
0.006
Biopsy performed at:
other hospital
our institution
2070 (448–9555) 0.351
Radiotherapy or
radiotherapy +chemotherapy
Chemotherapy alone or no
adjuvant therapies
* 0.094
*Radiotherapy odds ratio is not valuable.
Fig. 2 The Kaplan-Meier curve shows the survival without local
recurrence in patients with and without biopsy tract contamination.
Blue line = no contaminated biopsy tracts; green line = contaminated
biopsy tracts.
Volume 475, Number 2, February 2017 Biopsy Seeding and Relevance in Practice 515
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patients underwent percutaneous biopsies. At our center,
open biopsies were performed when we did not achieve a
diagnosis after at least two percutaneous procedures.
Thirty-eight percent of the biopsies were performed else-
where, consequently we cannot confirm the biopsy
technique in those patients. We obviously do not know
exactly why patients whose biopsies were performed at
outside centers received an open or a percutaneous biopsy,
but it is possible that patients with more-complicated or
less-accessible tumors underwent open biopsies, and this
could have accounted for some of the increased contami-
nation we observed with open biopsies. Even so, the open
biopsies performed at our center also showed a higher
contamination rate and the multivariate analysis showed
that the type of biopsy procedure (open or percutaneous)
was associated with the contamination, whereas the center
where the biopsy was performed did not correspond to the
contamination rate. Second, there was a relatively small
and heterogeneous group of patients with disparate diag-
noses that prevents statistical analysis of the effect of the
histologic diagnosis, and we also looked at bone and soft
tissue tumors together. In this series, we observed higher
contamination in soft tissue sarcomas compared with bone
sarcomas. Nevertheless, a larger study comprised of all
bone tumors or all soft tissue tumors might provide dif-
ferent results. Finally, we did not have enough patients who
received preoperative radiotherapy to determine if it might
have had an effect on contamination of the biopsy tract.
However none of the patients who received preoperative
radiation had contamination of the biopsy tract. This
variable should be cleared in further study.
The rate of biopsy tract seeding in our series was 12%.
There are some published cases of tumor recurrence in the
path of no resected or incompletely resected percutaneous
and open biopsy tracts [6,9,24,35]. Ribeiro et al. [23]
reported contamination of 32% of the biopsy tracts in the
largest series with 25 bone and soft tissue sarcomas.
Our study shows that the possibility of contamination is
present in open and percutaneous biopsies, but the likeli-
hood is greater with open than with percutaneous
procedures. This difference is independent of the hospital
where the biopsy is performed, as the possibility remained
when we compared percutaneous and open procedures
done at our center and at other centers. Other studies also
show a high risk of contamination of open biopsies
[18,23]. Saghieh et al. [25] reported 10 cases in pediatric
patients in which the percutaneous core needle biopsy tract
was not resected and the patients did not have any recur-
rence. Li et al. [12] suggested decreasing contamination of
the percutaneous biopsy tracts in patients with osteosar-
coma by using Adriamycin sponges.
When we looked for other factors associated with
contamination, we found that soft tissue sarcomas showed
higher biopsy tract contamination than bone sarcomas.
This factor may be related to the biopsy technique or to
the histologic characteristic of each tumor that could not
be analyzed separately in this study. Although in our
study this factor did not reach statistical significance,
other studies have indicated that radiotherapy may
decrease tumor tissue contamination near the biopsy
pathway [6,18,26]. Nevertheless more studies would be
necessary to define the influence of adjuvant therapies
(chemotherapy/radiotherapy). Binitie et al. [4] did not
address the relative effect of each of the adjuvant treat-
ments or the effect of these treatments in open biopsy
tracts. Moreover, they did not compare the local recur-
rence rate in their series with that of patients without
resected biopsies who did not receive any adjuvant
therapy.
In our study, the local recurrence-free survival was
higher in patients with contaminated biopsy tracts,
although with the numbers we had, we could not show a
difference in local recurrence-free survival in patients who
had percutaneous compared with open biopsies. We did not
show a difference, when considered separately, biopsies
performed at our institution and at other hospitals. It may
be attributable to the low number of open biopsies per-
formed at our center, but local recurrence is a complex
event that can be affected by other factors, therefore more
specific studies are needed to clarify these results.
Percutaneous core needle biopsies can cause contami-
nation in a resected biopsy tract, but the percentage of
Fig. 3 The Kaplan-Meier curve shows the survival without local
recurrence in patients with percutaneous and open biopsy tract
contamination. Blue line = percutaneous biopsy tracts; green line =
open biopsy tracts.
516 Barrientos-Ruiz et al. Clinical Orthopaedics and Related Research
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contaminated samples was much lower in our series than
with open biopsy, at our center and among patients referred
to us from outside centers for care. We found that patients
with a contaminated biopsy tract has shorter local recur-
rence-free survival than those with a noncontaminated
biopsy tract. This might indicate that wider margins are
needed around open biopsy tracts than was done in our
patients. Resecting the biopsy tract completely may be a
difficult task because its tridimensional shape may be dif-
ficult to predict reliably during the definitive surgery.
Jalgaonkar et al. [11] reported that the biopsy tract was
impossible to find after 3 months in 22 of 45 patients
(48.8%) when they did not mark it with India ink. With
open biopsies, the tridimensional shape of the scar is not
always as expected, and the hematoma, which may have
tumoral cells, can reach distant tissues. In our opinion,
although we can ascertain this proposition, we suspect we
are not able to completely resect a substantial number of
biopsy pathways.
The treating surgeon should assess the biopsy tract
carefully when planning definitive resection. More study is
needed to assess the potential benefits of adjuvant treat-
ments in preventing local recurrence, especially in patients
who have had an open biopsy. Percutaneous core needle
biopsies appear to be a safer approach to establishing the
diagnosis of a musculoskeletal neoplasm.
Acknowledgements We thank the biostatistics department of
Hospital La Paz, specially, Rosario Madero PhD, for contribution to
the analysis of the data in our study. We also thank Mar Tapia
Vin
˜edas MD (Radiology Department, University Hospital La Paz) for
her contribution to the biopsy procedures and Fernando Lopez-Barea
MD, PhD (Pathology Department, University Hospital La Paz) for his
contribution to the biopsy tract review.
References
1. Altuntas A, Slavin J, Smith P, Schlict S, Powell G, Ngan S, Toner
G, Choong PF. Accuracy of computed tomography guided core
needle biopsy of musculoskeletal tumours. ANZ J Surg.
2005;75:187–191.
2. Barrientos Ruiz I, Serrano Montilla J. Ortiz-Cruz EJ. [Cost
analysis of the diagnosis and treatment of soft tissue sarcomas in
reference centres][in Spanish]. Rev Esp Cir Ortop Traumatol.
2012;56:374–377.
3. Bickels J, Jelinek J, Shmookler B, Malawer M. Biopsy of Mus-
culoskeletal Tumors. In Malawer MM, Sugarbaker PH, eds.
Musculoskeletal Cancer Surgery Treatment of Sarcomas and
Allied Diseases. Dordrecht, The Netherlands: Kluwer Academic
Publishers; 2001:37–45.
4. Binitie O, Tejiram S, Conway S, Cheong D, Temple HT, Letson
GD. Adult soft tissue sarcoma local recurrence after adjuvant
treatment without resection of percutaneous core needle biopsies
tract. Clin Orthop Relat Res. 2013;471:891–898.
5. Campanacci M. Giant Cell Tumor. Bone and Soft Tissue Tumors:
Clinical Features, Imaging, Pathology and Treatment. 2nd ed.
Wien, Germany: Springer-Verlag; 1999:99–142.
6. Davies NM, Livesley PJ, Cannon SR. Recurrence of an
osteosarcoma in a needle biopsy track. J Bone Joint Surg Br.
1993;75:977–978.
7. De Marchi A, Brach del Prever EM, Linari A, Pozza S, Verga L,
Albertini U, Forni M, Gino GC, Comandone A, Brach del Prever
AM, Piana R, Faletti C. Accuracy of core-needle biopsy after
contrast-enhanced ultrasound in soft-tissue tumours. Eur Radiol.
2010;20:2740–2748.
8. Edge SB, Byrd DR, Compton CC, Fritz AG, Greene FL, Trotti A,
eds. AJCC cancer Staging Manual. 7th ed. New York, NY:
Springer; 2010.
9. Huang AJ, Kattapuram SV. Musculoskeletal neoplasms: biopsy
and intervention. Radiol Clin North Am. 2011;49:1287–1305.
10. Iemsawatdikul K, Gooding CA, Twomey EL, Kim GE, Goldsby
RE, Cohen I, O’Donnell RJ. Seeding of osteosarcoma in the
biopsy tract of a patient with multifocal osteosarcoma. Pediatr
Radiol. 2005;35:717–721.
11. Jalgaonkar A, Dawson-Bowling SJ, Mohan AT, Spiegelberg B,
Saifuddin A, Pollock R, Skinner JA, Briggs TW, Aston W.
Identification of the biopsy track in musculoskeletal tumour
surgery: a novel technique using India ink. Bone Joint J.
2013;95:250–253.
12. Li ZF, Li JM, Yan J, Yang ZP, Li X, Yang Q. Prevention of
contamination by biopsy needle track contamination using a
novel adriamycin-loaded gelatin sponge. World J Surg Oncol.
2013;11:169.
13. Liu PT, Valadez SD, Chivers FS, Roberts CC, Beauchamp CP.
Anatomically based guidelines for percutaneous core needle
biopsies of bone tumors: implications for limb-sparing surgery.
Radiographics. 2007;27:189–205; discussion 206.
14. Mankin HJ, Lange TA, Spanier SS. The hazards of biopsy in
patients with malignant primary bone and soft-tissue tumors. J
Bone Joint Surg Am. 1982;64:1121–1127.
15. Mankin HJ, Mankin CJ, Simon MA. The hazards of the biopsy,
revisited: members of the Musculoskeletal Tumor Society. J
Bone Joint Surg Am. 1996;78:656–663.
16. Mitton B, Seeger LL, Eckardt MA, Motamedi K, Eilber FC,
Nelson SD, Eckardt JJ, Federman N. Image-guided percutaneous
core needle biopsy of musculoskeletal tumors in children. J
Pediatr Hematol Oncol. 2014;36:337–341.
17. Mitsuyoshi G1, Naito N, Kawai A, Kunisada T, Yoshida A,
Yanai H, Dendo S, Yoshino T, Kanazawa S, Ozaki T. Accurate
diagnosis of musculoskeletal lesions by core needle biopsy. J
Surg Oncol. 2006;94:21–27.
18. Mohana R, Faisham W, Zulmi W, Nawfar AS, Effat O, Salzihan
MS. The incidence of malignant infiltration in the biopsy tract of
osteosarcoma. Malays Orthop J. 2007;1:7–10.
19. Narvani AA, Tsiridis E, Saifuddin A, Briggs T, Cannon S. Does
image guidance improve accuracy of core needle biopsy in
diagnosis of soft tissue tumours? Acta Orthop Belg. 2009;75:239–
244.
20. Oliveira MP, de Andrade Lima PM, DA Silva HJ, Viera de Mello
RJ. Neoplasm seeding in biopsy tract of the musculoskeletal
system: a systematic review. Acta Ortop Bras. 2014;22:106–110.
21. Pohlig F, Kirchhoff C, Lenze U, Schauwecker J, Burgkart R,
Rechl H, von Eisenhart-Rothe R. Percutaneous core needle
biopsy versus open biopsy in diagnostics of bone and soft tissue
sarcoma: a retrospective study. Eur J Med Res. 2012;17:29.
22. Puri A, Shingade VU, Agarwal MG, Anchan C, Juvekar S, Desai
S, Jambhekar NA. CT-guided percutaneous core needle biopsy in
deep seated musculoskeletal lesions: a prospective study of 128
cases. Skeletal Radiol. 2006;35:138–143.
23. Ribeiro MB, de Oliveira CR, Filippi RZ, Baptista AM, Caiero
MT, Saito CF, Barbosa do Nascimento SA, de Camargo OP.
Histopathological study on biopsy track in malignant muscu-
loskeletal tumors. Acta Ortop Bras. 2009;17:279–281.
Volume 475, Number 2, February 2017 Biopsy Seeding and Relevance in Practice 517
123
Author's personal copy
24. Robertson EG, Baxter G. Tumour seeding following percuta-
neous needle biopsy: the real story! Clin Radiol. 2011;66:1007–
1014.
25. Saghieh S, Masrouha KZ, Musallam KM, Mahfouz R, Abboud
M, Khoury NJ, Haidar R. The risk of local recurrence along the
percutaneous core-needle biopsy tract in patients with bone sar-
comas. Iowa Orthop J. 2010;30:80–83.
26. Schwartz HS, Spengler DM. Needle tract recurrences after closed
biopsy for sarcoma: three cases and review of the literature. Ann
Surg Oncol. 1997; 4:228–236.
27. Siegel GW, Biermann JS, Chugh R, Jacobson JA, Lucas D, Feng
M, Chang AC, Smith SR, Wong SL, Hasen J. The multidisci-
plinary management of bone and soft tissue sarcoma: an essential
organizational framework. J Multidiscip Healthc. 2015;8:109–
115.
28. Simon MA, Biermann JS. Biopsy of bone and soft-tissue lesions.
J Bone Joint Surg Am. 1993;75:616–621.
29. Skrzynski MC, Biermann JS, Montag A, Simon MA. Diagnostic
accuracy and charge-savings of outpatient core needle biopsy
compared with open biopsy of musculoskeletal tumors. J Bone
Joint Surg Am. 1996;78:644–649.
30. Sung KS, Seo SW, Shon MS. The diagnostic value of needle
biopsy for musculoskeletal lesions. Int Orthop. 2009;33:1701–
1706.
31. Verheijen P, Witjes H, van Gorp J, Hennipman A, van Dalen T.
Current pathology work-up of extremity soft tissue sarcomas:
evaluation of the validity of different techniques. Eur J Surg
Oncol. 2010;36:95–99.
32. Welker JA, Henshaw RM, Jelinek J, Shmookler BM, Malawer
MM. The percutaneous core needle biopsy is safe and recom-
mended in the diagnosis of musculoskeletal masses. Cancer.
2000;89:2677–2686.
33. Wu JS, Goldsmith JD, Horwich PJ, Shetty SK, Hochman MG.
Bone and soft-tissue lesions: what factors affect diagnosis yield
of image-guided core-needle biopsy? Radiology. 2008;248:962–
970.
34. Yang J, Frassica FJ, Fayad L, Clark DP, Weber KL. Analysis of
nondiagnostic results after image-guided needle biopsies of mus-
culoskeletal lesions. Clin Orthop Relat Res. 2010;468:3103–3111.
35. Zocalli C, Prencipe U, Erba F, Vidiri A, Di Filippo F. Biopsy can
determinate tumoral track contamination: a case report of chon-
drosarcoma. Eur J Radiol Extra. 2009;72:e79–e81.
518 Barrientos-Ruiz et al. Clinical Orthopaedics and Related Research
1
123
Author's personal copy
