Original Article

Core Needle Biopsy Versus Incisional Biopsy for Differentiation

of Soft-Tissue Sarcomas: A Systematic Review
and Meta-Analysis
1
Emrullah Birgin, MD ; Cui Yang, MD1; Svetlana Hetjens, DSc2; Christoph Reissfelder, MD1; Peter Hohenberger, MD1;
and Nuh N. Rahbari, MD1

BACKGROUND: Controversies exist regarding the biopsy technique of choice for the accurate diagnosis of soft-tissue sarcoma (STS).
The objective of this systematic review and meta-analysis was to compare the diagnostic accuracy of core needle biopsy (CNB) versus
incisional biopsy (IB) in STS with reference to the final histopathological result. METHODS: Studies regarding the diagnostic accuracy
of CNB and IB in detecting STS were searched systematically in the MEDLINE and EMBASE databases. Estimates of sensitivity and
specificity with associated 95% CIs for diagnostic accuracy were calculated. The risk of bias was assessed using the Quality Assessment
of Diagnostic Accuracy Studies version 2 (QUADAS-2). RESULTS: A total of 17 studies comprising 2680 patients who underwent 1582
CNBs and 241 IBs with subsequent tumor resection met the inclusion criteria. The sensitivity and specificity of CNB and IB to detect the
dignity of lesions were 97% (95% CI, 95%-98%) and 99% (95% CI, 97%-99%), respectively, and 96% (95% CI, 92%-99%) and 100% (95%
CI, 94%-100%), respectively. Estimates of the sensitivity and specificity of CNB and IB to detect the STS histotype were 88% (95% CI,
86%-90%) and 77% (95% CI, 72%-81%), respectively, and 93% (95% CI, 87%-97%) and 65% (95% CI, 49%-78%), respectively. Patients who
underwent CNB had a significantly reduced risk of complications compared with patients who underwent IB (risk ratio, 0.14; 95% CI,
0.03-0.56 [P ≤ .01). Quality assessment of studies revealed a high risk of bias. CONCLUSIONS: CNB has high accuracy in diagnosing the
dignity of lesions and STS histotype in patients with suspected STS with fewer complications compared with IB. Therefore, CNB should
be regarded as the primary biopsy technique. Cancer 2020;126:1917-1928. © 2020 American Cancer Society.

KEYWORDS: accuracy, dignity, histology, histotype, soft-tissue tumor (STS).

INTRODUCTION
Soft-tissue sarcomas (STS) are rare malignancies of mesenchymal origin.1 In Europe, the estimated incidence of STS
(excluding gastrointestinal stroma tumors) is up to 4 to 5 cases per 100,000 population per year.2,3 By nature, STS
are heterogeneous tumors encompassing >80 histological subtypes and the World Health Organization handbook lists
>75 intermediate and malignant STS types.4,5 This heterogeneity of tumor histology and genotype is associated with
marked differences in their clinical course and response to conventional and targeted anticancer treatments, requiring
refined treatment plans. Therefore, correct histological classification is mandatory before the initiation of individualized
treatment. In a potentially curative setting, the management of patients with STS frequently involves a multidisciplinary
approach including surgical resection with neoadjuvant and/or adjuvant (chemo)radiation protocols depending on histo-
logical classification and grade, tumor location, and size.6 In patients with locally advanced and metastatic STS, doxoru-
bicin-based chemotherapy remains the first-line treatment; however, in recent years, new, promising, and well-tolerated
targeted treatment agents have been developed for several STS subtypes.7-10
According to current European Society for Medical Oncology and National Comprehensive Cancer Network
guidelines, a biopsy of the primary tumor should be performed after cross-sectional imaging.11,12 The standard
approach is a core needle biopsy (CNB) or an open incision biopsy (IB) except for superficial lesions measuring
<3 cm, which might be considered for excisional biopsies. Although current clinical guidelines indicate CNB to be
the preferred technique over IB, controversies still exist among clinicians and pathologists regarding the diagnostic
accuracy of CNB.13,14 Two recent meta-analyses demonstrating a higher diagnostic accuracy for IB compared with

Corresponding Author: Nuh N. Rahbari, MD, Department of Surgery, Medical Faculty Mannheim, Mannheim School of Medicine, Heidelberg University, Theodor-Kutzer-
Ufer 1-3, 68167 Mannheim, Germany (nuh.rahbari@umm.de).
1
 Department of Surgery, Medical Faculty Mannheim, Mannheim School of Medicine, Heidelberg University, Mannheim, Germany; 2 Department of Medical Statistics and
Biomathematics, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany
We thank Dr. Linder for his advisory assistance in statistics.
Additional supporting information may be found in the online version of this article.

DOI: 10.1002/cncr.32735, Received: October 16, 2019; Revised: December 11, 2019; Accepted: January 9, 2020, Published online February 5, 2020 in Wiley Online
Library ­(wileyonlinelibrary.com)

Cancer   May 1, 2020 1917

Original Article
CNB have increased the controvery.15,16 However, these
analyses included lesions without a final surgical spec-
imen and bone sarcomas, even though chondroid and
bone lesions are characterized by a high rate of undiag-
nostic CNBs.17,18 Thus, this could result in the underes-
timation of the diagnostic accuracy of CNB in patients
with STS. Therefore, we performed a systematic review
of the literature and meta-analysis to determine the
diagnostic performance of both CNB and IB in patients
with resected STS.
MATERIALS AND METHODS
A systematic review of the literature was prepared in ac-
cordance with Preferred Reporting Items for Systematic
Reviews and Meta-Analyses (PRISMA) guidelines and
the Cochrane Handbook for Systematic Reviews of
Interventions.19,20
Search Strategy and Selection Criteria
A systematic literature search of the MEDLINE and
EMBASE databases was performed on October 1, 2018,
by 2 independent reviewers (E.B. and C.Y.) using vari-
ous combinations of the following terms: “sarcoma,”
“soft-tissue tumor,” “biopsy,” and “core needle.” The
detailed search strategies are provided in the Supporting
Information. The retrieved literature list (titles and
abstracts) was screened independently by 2 reviewers
(E.B. and C.Y.) for potential full-text eligibility. The
reference lists of relevant studies and reviews were cross-
checked for additional studies.
Studies that met the following criteria were in-
cluded: 1) the inclusion of patients who underwent
CNB and/or IB for suspicious soft-tissue masses prior to
definitive surgical resection; 2) the final histology of the
resected (surgical) specimen was used as the reference
standard for the preoperative biopsy; and 3) sufficient
data were reported to extract the number of true-
positive, false-positive, true-negative, and false-negative
results.
Studies were excluded if they were case reports or had
a total sample size of <10, if they reported on a biopsy
technique other CNB or IB, if the study cohort consisted
exclusively of patients with pathologies other than STS (eg,
bone sarcoma or benign lesions), and if they were non–peer-
reviewed or nonhuman studies. In the case of disagreements,
a third author (N.N.R.) was consulted for discussion.
Data Extraction
Two authors (E.B. and C.Y.) independently extracted
data using structured data collection forms and captured
1918
the following variables of interest: first author, year of
publication, country of origin, study design, and study
period. Furthermore, we extracted study group charac-
teristics such as the total number of patients; the mean
or median age (with the SD or range); the male-to-
female ratio; the biopsy method; and, if available, details
regarding the biopsy technique, details of the patholo-
gists, use of histological grading system, cost analyses,
referral center, postprocedural complications, and the
need for repeated biopsies. In the case of disagreements,
differences were resolved by discussion. The surgical
specimen was used as the reference standard and 2 × 2
contingency tables were extracted or reconstructed for
CNB and IB in every included study for the diagnostic
accuracy of the dignity and the final histological diag-
nosis, respectively.
Assessment of Study Quality
Methodological quality was assessed individually by 2
authors (E.B. and C.Y.) using the Quality Assessment of
Diagnostic Accuracy Studies (QUADAS) tool.21
Statistical Analysis
Estimates of sensitivity and specificity (including 95%
CIs) for the index tests (CNB and IB) and their correla-
tion to the final histological diagnosis as well as to the
dignity of the lesions (malignant, benign) were calculated
from the extracted contingency tables. Individual study
estimates were plotted in the receiver operating character-
istic (ROC) space. Hierarchical summary ROC plots were
obtained using hierarchical logistic regression modeling
and summary plots were drawn. Heterogeneity between
studies was examined by evaluating the following factors
potentially affecting the diagnostic accuracy: year of pub-
lication, details regarding withdrawals from the study (yes
or no), detailed description of the resected specimen (yes
or no), reporting of inconclusive tests (yes or no), and
prevalence of STS. Subgroup analysis to identify factors
affecting diagnostic accuracy was performed by plotting
summary ROC curves after logistic regression if ≥4 stud-
ies were included for comparison. To calculate binary
outcomes and risk ratios (RRs) with 95% CIs, random
effects models were used because interstudy heterogeneity
was expected between the studies. Chi-square tests with
the statistical significance set at P < .05 were performed
to analyze interstudy heterogeneity. Pooled estimates of
sensitivity and specificity were calculated using MetaDisc
1.4 software. Statistical analysis was performed in Review
Manager Version 5.2 (Cochrane Collaboration) and SAS
(version 9.4) statistical software.
Cancer   May 1, 2020

Figure 1. Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) flow chart. CNB indicates core needle
biopsy; IB, incisional biopsy; STS, soft-tissue sarcoma.
RESULTS
The systematic literature search yielded a total of 1659
articles, with 28 additional articles identified through
screening the reference lists of the included studies.
Duplicate articles were removed and studies were scanned
for eligibility. A final total of 17 studies met the inclusion
criteria for meta-analysis. Figure 1 presents the flow chart
according to the PRISMA guidelines.
Study Characteristics
The main characteristics of the studies are summarized
in Table 1.22-38 The publication year of the included
Cancer   May 1, 2020
Sarcoma Biopsy Method/Birgin et al
studies ranged from 1998 to 2018. Overall, 2680
patients underwent 2720 biopsies, among whom
2190 CNBs and 319 IBs were performed. In addition
to CNB or IB, fine-needle aspiration (FNA) biopsies
were conducted in 4 studies22-25 and 2 studies reported
excisional biopsies25,26 as additional biopsy techniques.
Patients underwent multiple biopsy sessions in 2 stud-
ies.22,27 Five studies provided information regarding
both CNB and IB.22,24,25,28,29
Of all the reported patients, the mean age was
55 years (range, 12-95 years) with a male predominance
(55%). Histological details of the resected specimens
1919
Original Article

TABLE 1.  Study Characteristics of the Included Studies

Age, Years Biopsy Method

Study Sex Median Mean

Study Country Period No. of Patients M:F (Range) (SD) Total CNB, % IB, %
27 a a
Colletti 2016 Japan 2009-2015 213 116:99   NA (12-95) 60 215   215 (100) 0
Coran 201532 Italy 2012-2014 40 22:18 NA (25-88) 58 40 40 (100) 0
Hoeber 200125 UK 1989-1998 570 NA NA NA 576b  314 (55) 56 (10)
Issakov 200334 Israel 1998-2000 215 131:84 NA (14-86) NA 215 215 (100) 0
Kasraeian 201024 US 2007-2009 57 33:23c  NA 57 57 57 (100) 57 (100)
Kiatisevi 201328 Thailand 2008-2010 176 83:93 NA NA 176 112 (64) 64 (36)
Layfield 201422 US NA 257 NA NA (19-96) 54 303d  130 (43) 111 (37)
Lin 201636 US NA 53 25:28 62 (23-91) NA 53 53 (100) 0
Liu 200437 China 1999-2000 37 21:16 NA (13-82) 49 37 37 (100) 0
De Marchi 201038 Italy 2007-2008 115 NA NA NA 115 115 (100) 0
Noebauer-Huhmann 201530 Austria NA 42 24:18 NA (19-84) 52 42 42 (100) 0
Pohlig 201229 Germany 2007-2008 77 NA NA NA 77 46 (60) 31 (40)
Seng 201333 Singapore 1990-2008 134 NA NA NA 134 134 (100) 0
Serpell & Pitcher 199826 Australia 1991-1996 45 21:24 NA (20-90) 53 31 31 (100) 0
Strauss 201031 US 2004-2008 530 NA NA NA 530 530 (100) 0
Walker 201835 US 2011-2017 69 38:31 NA 55 (19) 69 69 (100) 0
Yang & Damron 200423 US NA 50 30:20 NA NA 50 50 (100) 0

Abbreviations: CNB, core needle biopsy; F, female; IB, incision biopsy; M, male; NA, not available.
a
Two patients had 2 lesions.
b
A total of 180 patients underwent excision biopsies, 9 patients underwent fine-needle aspiration, and 17 had no further specified method of diagnosis.
c
One patient had missing information.
d
Included patients had multiple biopsies and 62 patients underwent fine-needle aspiration.

were available for a total of 2054 lesions across all stud-
ies. Of these, 1388 lesions (68%) were malignant and
1192 (58%) were identified as STS. Prior to surgical
resection, a total of 1582 CNBs and 241 IBs were per-
formed, which represented the final study cohort for
meta-analysis.
Risk of Bias and Quality Assessment
The risk of bias assessment demonstrated a high risk of
bias among the included studies (Fig. 2).22-38 All included
trials were single-center studies with a retrospective
design, with the exception of 3 prospective studies.23,24,30
Of these, 2 studies had cross-sectional study designs
with simultaneous CNB and IB24 or simultaneous
CNB and FNA performed in the same individual.23
The clinical setting of the biopsy techniques was hetero-
geneous within and across studies (Table 2).22-38 Seven
studies25,28,30-34 reported a single pathologist assessing the
samples, whereas >1 pathologist was involved in 6 stud-
ies.22,24,27,29,35,36 No information regarding the patholo-
gists analyzing the samples was given in 4 studies.23,26,37,38
Eleven studies23,24,26-28,30,31,33,36-38 described the refer-
ence standard (final histology) in detail (see Supporting
Table 1). Six studies23,25,30,31,36,38 provided information
regarding the malignancy grade, although only 2
studies31,36 mentioned the use of the National Federation
of Cancer Centers (Federation Nationale des Centres
de Lutte Contre le Cancer; FNCLCC) grading system.
Three studies22,25,36 gave no details regarding patient
withdrawals. An STS prevalence of >50% was present
in 9 studies.22,25-27,30,31,33,36,38 No study described cost
analysis associated with CNB or IB.
Nondiagnostic Samples
Of all reported biopsies, the rate of nondiagnostic sam-
ples after CNB and IB ranged from 0% to 10% and 0%
to 4%, respectively (Table 3).22-38 The pooled rate of
nondiagnostic samples among STS cases after CNB was
2% (7 of 433 cases), whereas all IBs yielded a diagnosis.
Comparative data for nondiagnostic samples using both
biopsy techniques were available in 4 studies,22,24,28,29
although only 3 of these24,28,29 revealed distinct data for
nondiagnostic STS. Meta-analysis of these studies dem-
onstrated no significant difference between CNB and IB
with reference to all reported samples (RR, 1.81; 95% CI,
0.75-4.36 [P = .19; I2 = 0%]) and with reference to STS
(RR, 3.07; 95% CI, 0.50-18.84 [P = .23; I2 = 0%]) (see
Supporting Fig. 1). Pathological details regarding nondi-
agnostic samples were available in 5 studies,23,24,26,28,38
and these were described as follows: 6 inadequate sam-
ples (final diagnosis: chondroblastoma, fibrosarcoma,
liposarcoma, desmoid tumor, arteriovenous malforma-
tion, and ancient schwannoma), 5 samples with necrotic
tissue (final diagnosis: 2 cases of multiple myeloma,

1920 Cancer   May 1, 2020


Figure 2. Risk of bias assessment. Quality assessment of the included studies according to Quality Assessment of Diagnostic
Accuracy Studies Version 2 (QUADAS-2) criteria.22-38
1 giant cell tumor, 1 well-differentiated liposarcoma, and
1 inclusion dermoid), cartilage with atypical cells (final
diagnosis: chondrosarcoma), nonspecific spindle cell
lesion (final diagnosis: malignant peripheral nerve
sheath tumor), atypical cells (final diagnosis: squamous
cell carcinoma), 2 samples with skeletal muscle (final
diagnosis: tuberculous myositis and myositis ossificans,
respectively), fibrin (final diagnosis: Charcot arthropathy),
Cancer   May 1, 2020
Sarcoma Biopsy Method/Birgin et al
bony tissue with atypical cells (final diagnosis: parosteal
osteosarcoma), and insufficient material (final diagnosis:
nodular fasciitis and hemangioma).
Meta-Analysis of Accuracy
for the Diagnosis of Malignancy
Meta-analysis was performed for a total of 15 stud-
ies22-28,30-35,37,38 to differentiate the correct dignity of
1921
Original Article

TABLE 2.  Characteristics of Biopsy Technique, Repeat Procedures, and Pathological Evaluation

Repeat
CNB Technical Characteristics Procedures Pathological Evaluation

Study Modality Needle, Gauge Sample No. CNB IB Pathologists Grading System Referral Center
27
Colletti 2016 CT, US 18, 20 NA NA — Multiple (expert) NA Yes
Coran 201532 US 14 2-3 NA — Single NA Yes
Hoeber 200125 NA NA NA NA NA Single Yes (NA) Yes
Issakov 200334 CT 14, 18 5-10 3/80 — Single NA Yes
Kasraeian 201024 NA NA 4-6 NA NA Multiple (expert) NA No
Kiatisevi 201328 CT 14 6-10 7/112 3/64 Single NA No
Layfield 201422 NA NA NA NA NA Multiple (expert) NA Yes
Lin 201636 CT, US 16-20 2-4 NA — Multiple (expert) Yes (FNCLCC) Yes
Liu 200437 US 14, 16, 18 3-6 NA — NA No No
De Marchi 201038 US 16, 18 NA NA — NA Yes (ESMO) Yes
Noebauer-Huhmann 201530 MRI 14 3-4 NA — Single (expert) Yes (WHO) Yes
Pohlig 201229 CT, US 14 3-5 NA NA Multiple (expert) NA Yes
Seng 201333 CT NA 3-5 NA — Single (expert) No Yes
Serpell & Pitcher 199826 Variable NA NA NA — NA NA No
Strauss 201031 Freehand NA 4 37/530 — Single (expert) Yes (FNCLCC) Yes
Walker 201835 NA NA NA NA — Multiple (expert) NA No
Yang & Damron 200423 NA 22 6 NA — NA Yes (NA) No

Abbreviations: CNB, core needle biopsy; CT, computed tomography; ESMO, European Society for Medical Oncology; FNCLCC, National Federation of Cancer
Centers (Federation Nationale des Centres de Lutte Contre le Cancer); IB, incision biopsy; MRI, magnetic resonance imaging; NA, not available; US, ultrasound;
WHO, World Health Organization.

TABLE 3.  Summary of Diagnostic Outcome in Included Studies

Bx Method Prior to
Nondiagnostic Samples Final Diagnosis of Resected Specimen Resection

CNB IB

Study Total STS Total STS Total Benign Malignant STS Total CNB IB
27
Colletti 2016 NA NA — — 161 23 138 138 161 161 0
Coran 201532 0/40 0/8 — — 27 19 8 8 27 27 0
Hoeber 200125 7/314 NA NA NA 303a  84 216 216 300 257b  43c 
Issakov 200334 22/215d  2/25 — — 80 45 35 25 80 80 0
Kasraeian 201024 2/57 1/19 0/57 0/57 57 26 31 19 57e  57e  57e 
Kiatisevi 201328 8/112 1/16 2/64 0/14 176 85 91 30 30 16 14
Layfield 201422 6/130 NA 4/111 NA 257 54 203f  203 241 130 111
Lin 201636 0/53 0/53 — — 53 0 53 53 53 53 0
Liu 200437 1/37 0/16 — — 37 13 24 16 37 37 0
De Marchi 201038 6/115 2/61 —   115 41 74 61 103 103 0
Noebauer-Huhmann 201530 0/42 0/29 — — 42 11 31 29 42 42 0
Pohlig 201229 1/46 1/13 0/31 0/16 77 0 77 29 29 13 16
Seng 201333 7/134g  NA — — 134g  32 102 72 85 85 0
Serpell & Pitcher 199826 1/36 0/25 — — 45 20 25 25 31 31 0
Strauss 201031 37/530 NA — — 371 155 216 216 371 371 0
Walker 201835 0/69 0/31 — — 69 38 31 31 69 69 0
Yang & Damron 200423 1/50 0/21 — — 50 17 33 21 50 50 0
Total 99/1980 7/433 6/263 0/87 2054a  663 1388 1192 1766 1582 241

Abbreviations: Bx, biopsy; CNB, core needle biopsy; IB, incision biopsy; NA, not available; STS, soft-tissue sarcoma.
a
Three patients were excluded from further analysis due to the wrong diagnosis given on CNB or IB.
b
Fifty-five patients were excluded from the initial cohort (21 patients for receipt of treatment other than surgical resection, 13 patients for a benign diagnosis, 11
patients for other malignancies, 7 patients for technical failures, 2 patients for receipt of prior neoadjuvant therapy, and 1 patient for unresectable disease).
c
Twelve patients were excluded from the initial cohort (3 patients for receipt of prior neoadjuvant treatment, 6 patients for no surgical resection, 2 patients for no
STS, and 1 patient for unresectable disease).
d
A total of 135 bony lesions were included; among soft-tissue tumors only 5 of 80 (6%) nondiagnostic samples were present.
e
All patients underwent simultaneous CNB and IB.
f
Four samples were characterized as “indeterminate dignity” in the final pathology but were counted as a malignant lesion.
g
Three samples had a benign bone tumor, 30 had a malignant bone tumor, and 16 tumors were benign inflammatory lesions.

1922 Cancer   May 1, 2020

 Sarcoma Biopsy Method/Birgin et al

Figure 3. Diagnostic accuracy of lesion dignity and of soft-

tissue sarcoma (STS) histotype. Hierarchical summary receiver
operating characteristic (HSROC) plots for (A) lesion dignity
and (B) STS histotype are shown. The data from each study
are represented by a circle (core needle biopsy [CNB]) or
diamond (incisional biopsy [IB]) in HSROC plots. Forrest
plots of sensitivity and specificity are shown with 95% CIs. FN
indicates false-negative; FP, false-positive; TN, true-negative;
TP, true-positive.22-28,30-38

samples (Fig. 3A).22-28,30-38 Estimates for sensitivity were

pooled for the study groups and calculated as 97% (95%
CI, 95%-98%) in the CNB group and 96% (95% CI,
92%-99%) in the IB group (see Supporting Figs. 2A and
2B). The specificity analysis demonstrated a pooled speci-
ficity rate of 99% (95% CI, 97%-99%) after CNB and
100% (95% CI, 94%-100%) after IB. In the CNB study
groups, covariate subgroup analysis yielded comparable
results for the number of pathologists analyzing biop-
sies and the assessment of samples in referral centers (see
Supporting Fig. 3).

Meta-Analysis of Accuracy for STS Histotype

A total of 13 studies22,23,25-28,30-34,37,38 were included in
the meta-analysis for the diagnosis of the STS histotype
(Fig. 3B).22-28,30-38 The sensitivity estimates of CNB and
IB were pooled and calculated as 88% (95% CI, 86%-
90%) and 93% (95% CI, 87%-97%), respectively (see
Supporting Figs. 2C and 2D). The pooled specific-
ity estimates were 77% (95% CI, 72%-81%) and 65%
(95% CI, 49%-78%), respectively, in the CNB and IB
groups. Figure 3B shows the funnel plot and ROC curve
analysis.22-28,30-38 A covariate subgroup analysis demon-
strated higher diagnostic accuracy in the case of single
pathologists analyzing samples and the assessment of sam-
ples in referral centers (see Supporting Fig 3).

Meta-Analysis of Biopsy-Related Complications

Eight studies24,25,28-31,34,35 reported complications
after CNB and IB, with a pooled complication rate
of 1% (10 of 1034 cases) in comparison with 4% (8
of 195 cases), respectively. Complications are detailed
in Table 4.24,25,28-31,34,35 A meta-analysis of compara-
tive studies reporting complications demonstrated a
significantly reduced risk of complications after CNB
(RR, 0.14; 95% CI, 0.03-0.56 [P  ≤  .01; I2  =  0%])
(see Supporting Fig. 4).

Meta-Analysis of the Need

for Repeat Procedures
Three studies28,31,34 described the need for repeated
biopsies after nondiagnostic CNB or IB. Overall, 50 of

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Original Article

TABLE 4.  Complications After CNB and IB

CNB IB

Secondary
Complications Intervention Complications Secondary Intervention

Study No. Details No. Details No. Details No. Details

Hoeber 200125 0/257 — 0/0 — 3/43   NA —
Issakov 200334 3/80 Hematoma 0/3 — —   —  
Kasraeian 201024 1/57a  Wound breakdown 0/1 — 1/57a  Wound breakdown 0/1 —
Kiatisevi 201328 1/112 Hematoma 1/1 Excision 3/64 2 cases of wound break- 3/3 2 cases of
down, hematoma debridement,
excision
Noebauer-Huhmann 201530 1/42 Bleeding 0/1 — —   —  
Pohlig 201229 0/46 — 0/0 — 1/31 Wound breakdown 0/1  
Strauss 201031 2/371 Hematoma, bleeding 1/2 Laparotomy        
Walker 201835 2/69 Hematoma, bleeding 1/2 Skin suture        

Abbreviations: CNB, core needle biopsy; IB, incision biopsy; NA, not available.
a
Same patient.

786 patients (6%) required a repeat biopsy. Of these, 47
patients underwent CNB compared with 3 patients who
underwent IB as their primary biopsy technique. Details
regarding the repeat procedures were described in only
2 studies and patients underwent secondary CNB or
IB.28,34
DISCUSSION
IB has long been considered the gold standard for the
diagnosis of STS. However, open surgical biopsy often
resulted in wound complications, tumor spreading,
and inappropriate incisions, even rendering subsequent
surgical resection more difficult.39,40 This led to the
development of less invasive percutaneous methods
using image-guided needles to gain adequate tissue for
pathological diagnosis. To differentiate histological sub-
types and the grading of STS, CNB evolved as an alter-
native to open techniques, providing sufficient tissue
for histopathological and immunohistochemical evalu-
ation.41 In the early 2000s, FNA often was discussed as
an alternative to CNB. However, this technique only
provides cytology without the distinct features of tis-
sue architecture.42 Therefore, current clinical practice
guidelines only recommend biopsy via core needle as
the standard or open IB and restrict FNA to use in re-
ferral centers with specific expertise.11,12 CNB appears
to be a cost-effective method that can be managed in
an outpatient service, whereas IB has to be performed
in an operating theater but provides large sample vol-
umes with a potentially higher diagnostic accuracy.38
To investigate this diagnostic dilemma, we performed a
meta-analysis regarding the diagnostic performance of
CNB and IB in resected STS.
The results of the current meta-analysis demon-
strated that CNB is not inferior to IB in diagnosing the
correct STS histotype. Furthermore, CNB is associated
with fewer complications compared with IB. We cor-
related diagnostic accuracy of the STS histotype with
the final histological specimen (reference standard) and
excluded those studies evaluating diagnostic accuracy
without correlation to the final surgical specimen.
In total, we found more nondiagnostic samples in
the CNB group compared with the IB group. However,
this was not reflected in comparative studies between
both study groups. In CNB, nondiagnostic samples can
arise due to technical errors and the histological het-
erogeneity of tumors.43 Therefore, multiple cores using
≥14-gauge needles from different tumor locations and
depths in correlation with radiological imaging should
be performed according to the current guidelines.12 The
current analysis indicated that a variety of needle gauge
sizes ranging from 8-gauge to 22-gauge needles and num-
ber of passes ranging from 2 to 10 were applied across
the included studies. Unfortunately, we were unable to
analyze the impact of needle gauge size and number of
passes on diagnostic accuracy due to heterogenous reports
among the studies that prohibited further meta-analysis.
At the study institution, we recommend at least 3 passes
for CNB using 14-gauge or 16-gauge needles. However,
to the best of our knowledge, there is no prospective trial
to date assessing different needle sizes for STS and its di-
agnostic accuracy in the literature. It is interesting to note
that 2 cross-sectional studies in the current meta-analysis
included patients with sequential biopsies in the same
individual, which might negatively affect diagnostic
accuracy. In fact, patients underwent CNB after FNA
in the study by Kasraeian et al,24 whereas the study

1924 Cancer   May 1, 2020


by Yang and Damron23 included patients who under-
went FNA after CNB. Thus, the results of the present
meta-analysis demonstrated high interstudy and intras-
tudy differences in CNB techniques. In the case of non-
diagnostic samples, the biopsy algorithm was guided by
higher invasiveness to achieve a diagnosis.22
Although several covariates with a potential im-
pact on diagnostic performance were identified in the
current study, meta-analyses were found to be feasible
only in the CNB group for 2 covariates. We concluded
that the assessment of samples by a single pathologist
as well as the performance of studies in referral centers
were associated with a higher diagnostic performance,
which might well be the result of an established work-
flow between radiologist, surgeon, and pathologist.
Nevertheless, one has to consider that it is the expertise
of the pathologists (eg, special training in the assess­
ment of soft-tissue mass biopsies), rather than the
number of pathologists, that might reflect a sufficient
quality criterion. However, heterogeneous definitions of
“expert pathologists” in the included studies prevented
further subgroup analyses. In addition, the STS grading
systems were used heterogeneously in the studies and
subgroup analysis of the accuracy of malignancy grad-
ing was not feasible. It is important to remember that
many pathologists refuse to assess the grading of an STS
from a CNB due to sampling errors and will provide
it only after having reviewed the resection specimen.
Nevertheless, pathological expert validation is encour-
aged in the case of an STS diagnosis outside of referral
or network centers for sarcomas.44 In fact, in up to one-
third of STS cases for which the diagnosis was made by
general pathologists, the final diagnosis was revised if
the case was reviewed by an STS pathologist.45,46 This
most likely is due to the individual expertise of dedi-
cated sarcoma pathologists with frequent exposures to
soft-tissue tumors as well as the overall general labo-
ratory expertise in dealing with sarcoma specimens.47
Indeed, the availability and standardization of specific
immunohistochemical or molecular assays are pivotal
in the case of an uncertain diagnosis. Consequently,
the results of the current study have highlighted the
important role of dedicated pathologists in the man-
agement of patients with STS because correct pathol-
ogy may have prognostic and predictive relevance. In
addition, we recommend that STS management be pro-
vided in sarcoma centers because this is associated with
a better quality of pathologic reports and oncological
outcomes.48 Overall, careful planning of a pretreatment
biopsy should be performed in a multidisciplinary
Cancer   May 1, 2020
Sarcoma Biopsy Method/Birgin et al
setting between surgeons, radiologists, and pathologists.
After cross-sectional imaging, it is pivotal to determine
the correct access point to the lesion with reference to
future surgical resection and the relation of the lesion
to neurovascular and visceral structures without com-
promising anatomical compartments.49 It is important
to obtain representative tissue samples from peripheral
areas rather than central necrotic areas. Furthermore,
areas that appear to be of a higher tumor grade on
cross-sectional imaging should be biopsied. Because
surgical resection of the needle tract is a common prac-
tice among surgical oncologists to reduce the potential
risk of needle tract seeding, the biopsy location needs
to be addressed when performing biopsy to the correct
part of the tumor. To our knowledge, no included study
herein assessed needle tract seeding and metastasis after
CNB. The evidence of needle tract metastasis, however,
is a conflicting topic because it is based solely on case
reports and retrospective cohort studies with an esti-
mated incidence of <1%.50 Although studies have sug-
gested that patients who underwent percutaneous biopsy
for sarcoma are not at higher risk of developing local
recurrence or needle tract metastasis, the use of het-
erogeneous biopsy techniques without differentiating
between open or percutaneous biopsy with or without
coaxial needles, data pooling of different sarcoma enti-
ties (mixing up bone sarcoma and STS or histological
grading), and an overall limited number of cases of nee-
dle tract metastasis does not allow for definitive conclu-
sions.49,51-53 In recent years, the use of coaxial sheathed
biopsy needles has reduced the risk of malignant cell
deposits in the needle tract.54 Even in the case of
retained malignant cells, their clinical significance remains
unclear in the era of modern perioperative chemoradi-
ation. It is a prerequisite to consider the location of the
needle trajectory when planning CNB, although this
might not be essential for patients with retroperitoneal
STS because surgical resection of retroperitoneal STS
typically is accomplished transperitoneally, leaving the
needle tract in situ. It is interesting to note that a recent
large cohort study depicted an incidence of needle tract
metastasis of 0.5% in patients with retroperitoneal
STS after a median follow-up of 44 months.55 Another
recent study comparing needle tract resection in patients
with extremity STS found no significant difference with
regard to recurrence rates compared with patients with-
out needle tract excision.56 In summary, pretreatment
biopsy does not compromise oncological outcomes but
the decision to perform biopsy should be discussed in a
multidisciplinary setting with reference to location on
1925
Original Article
cross-sectional imaging, biopsy technique, and individ-
ual patient characteristics.
Overall, we noted a high risk of bias in the included
studies because to our knowledge there as yet are no
prospective randomized controlled trials available in the
literature.
Across the studies, all bleeding complications and
hematomas (except for one case of a skin hematoma)
were observed after CNB, whereas all reported wound
breakdowns and impaired wound healings were observed
after IB. In the CNB group, one case of bleeding was
managed by simple skin suturing and one case required
a semiurgent laparotomy for tumor resection 3 days after
CNB was performed.31 Secondary surgery for wound
debridement and wound closure (2 patients) after IB was
reported in only 1 study.28 The study by Hoeber et al pro-
vided no detailed information regarding 3 cases of wound
breakdowns after IB.25
There are several potential limitations to this
meta-analysis. The sample size of the included patients
who underwent IB was rather small and prohibited fur-
ther subgroup analysis. Not all studies were included for
meta-analyses of diagnostic accuracy for dignity of the
lesions and for STS histotype, respectively. This mainly
was due to missing specificity estimates in some studies.
The study by Kasraeian et al24 was excluded from analysis
of STS histotype and dignity in the CNB group due to
a high risk of bias because all patients underwent CNB
immediately after FNA. Of note, Kasraeian et al24
reported 1 CNB of a well-differentiated liposarcoma that
yielded necrotic material, potentially due to the sequential
biopsy algorithm because necrosis is very unlikely in well-
differentiated liposarcoma.
In addition, different biopsy techniques were used in
the CNB group, which might have affected the frequency
of nondiagnostic samples and postinterventional compli-
cation rates. Unfortunately, the included studies demon-
strated scarce data concerning repeat procedures. There was
a high risk of bias with regard to patient selection and to
flow and timing in the included studies, although there was
a low risk of applicability concerns. This mainly was due
to the retrospective nature of the majority of studies, with
potential significant selection bias and varying study sizes.
Analyzing the data from Table 1 further and limiting them
to reports regarding >100 patients, 5 of the 8 centers did
not perform IBs. The CNB-to-IB ratio was 10:1 in these
studies compared to 3:1 in the remaining reports, indicat-
ing a clear disbalance of experience. Furthermore, these
data outlined the clear shift in large referral centers toward
CNB. However, in clinical practice, we still encounter a
1926
great deal of cases with incorrect and unplanned IBs (eg,
large transverse incisions) as the primary biopsy technique
performed outside of referral centers. This mainly is due
to the lack of the above-mentioned multidisciplinary
teams outside of referral centers. Although CNB should be
regarded as the primary biopsy technique for patients with
suspected STS, several studies have reported a low diagnos-
tic yield in the case of bony tissues.17,57 Because the bone
cortex could limit needle penetration to achieve adequate
samples, IB might be the preferred technique in this setting
after individual assessment. One also has to consider the
preferred biopsy technique in the case of cystic, vascular,
or exulcerated tumors. Nevertheless, there always is the
option to amend CNB by IB in the case of insufficient
sampling, but this is not always true for the reverse.
The ideal biopsy technique should be simple and
characterized by a high diagnostic accuracy while having
reasonable morbidity with limited tumor spread. Within
the above-mentioned limitations, the current meta-
analysis found CNB to be the superior method with
which to differentiate STS subtype, with lower com-
plications compared with IB. Because of the very high
diagnostic accuracy rates noted with both techniques and
a significantly higher invasiveness of IB with the need for
general anesthesia, it will be difficult to justify random-
ized trials comparing both methods.
FUNDING SUPPORT
No specific funding was disclosed.
CONFLICT OF INTEREST DISCLOSURES
The authors made no disclosures.
AUTHOR CONTRIBUTIONS
Study conception and design: Emrullah Birgin and Nuh N. Rahbari.
Collection and assembly of data: Emrullah Birgin and Cui Yang. Analysis
and interpretation of data: Emrullah Birgin, Svetlana Hetjens, and Nuh
N. Rahbari. Drafting of the article: Emrullah Birgin. Critical revision:
Christoph Reissfelder, Peter Hohenberger, and Nuh N. Rahbari.  The
dataset generated during the current study is available from the correspond-
ing author upon request.
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