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Int J Clin Exp Med 2016;9(8):16703-16709 /ISSN:1940-5901/IJCEM0029876
Original Article
Analysis of false negative rate in sentinel lymph node
biopsy of breast cancer: a single centre retrospective
study from China
Xinzhao Wang1*, Zhaoyun Liu1*, Qian Yu2, Nana Xu3, Leilei Wang1, Qinghua Ma1, Zhiyong Yu1
Shandong Cancer Hospital and Institute, Jinan, China; 2Department of Biology Winship Cancer Institute, Emory
University, Georgia, USA; 3The Fifth People’s Hospital of Jinan, Jinan, China. *Equal contributors.
Received April 5, 2016; Accepted July 3, 2016; Epub August 15, 2016; Published August 30, 2016
Abstract: Sentinel lymph node biopsy substituting axillary lymph node dissection has become a routine surgery
in many countries but not in China because of the false negative rate. False negative (FN) of sentinel lymph node
(SLN) can lead an incorrect assessment of pathological staging. In this study, we retrospectively analyzed the clinic
pathological data of 645 breast cancer patients in Shandong Cancer Hospital and Institute from January 2012 to
December 2015. True positive (TP), True negative (TN) and FN were identified in 383 patients (59.4%), 215 patients
(33.3%) and 39 patients (9.2%), respectively. Among FN patients, about 92.3% of them were found that the positive
lymph nodes were in Level I and/or Level II. Negative predictive value was 96.4% (215/223). Accuracy rate was
92.7% (494/598). FN rate was likely to occur in patients who were estrogen receptor (ER) negative, progesterone receptor (PR) negative, human epidermal growth factor 2 (HER2) positive and less than 3 positive axillary lymph nodes
(all P<0.05). Among these four molecular subtypes, HER2-enriched subtype is more likely to be FN (P=0.001).
A multivariate logistic regression model confirmed that ER status (OR=0.124, P<0.05), HER2 status (OR=3.703,
P<0.05) and the numbers of positive lymph nodes (OR=0.009, P<0.05) were all independent factors predicting FN
results. For those patients with high risk factors, such as ER negative, PR negative and HER2 positive, dissection of
Level I and Level II lymph node may be a relatively safe measure, considering the limited medical conditions, such
as unskilled surgeons and poor equipment conditions.
Keywords: Breast neoplasm, sentinel lymph node biopsy, false negative, axillary lymph node dissection
Breast cancer is the most common malignant
tumor and the leading cause of cancer death in
female patients. Lymph node metastasis is one
of the most important prognostic factors in
breast cancer and lymph node status is a major
determinant of treatment strategy for early
breast cancer. Sentinel lymph node (SLN) is
defined as the first chain node in the lymphatic
vessel which receives primary lymphatic flow. If
the SLN is negative, then other nodes are
expected to be disease-free. In order to decrease morbidity associated with lymph node
dissection, such as limb edema, numbness
and activity limitation, the technology of sentinel lymph node biopsy (SLNB) was first reported in the 1990s [1, 2]. Many labeling methods,
such as blue dyes and radiocolloid tracers
alone or in combination, were introduced to
identify the SLN. SLNB was accepted as a standard for T1-2 breast cancer undergoing breast
surgery without clinical palpable lymph nodes
after large clinical trials indicated considerably
clinical benefit in many countries [3-6].
Many researchers have conducted follow-up
studies to identify the significance of false-negative (FN) results [7, 8]. It is known that identification of lymph node status plays a far-reaching
implication on postoperative management and
adjuvant therapy in breast cancer. The FN rate
defines the frequency with which the sentinel
lymph nodes are pathologically negative but in
the presence of other positive axillary nodes. In
most area of China, SLNB rather than axillary
lymph node dissection (ALND) is not a routine
operation. Incomprehension of the axillary
False negative in sentinel lymph node biopsy of breast cancer
Table 1. Analysis of clinical and pathological
characteristics of breast cancer patients
Age at dignosis
>49 yares
≤49 years
Menopause status
Post menopausal
ER status
PR status
HER2 status
Ki-67 expression
Histopathological type
Invasive ductal carcinoma
Invasive lobular carcinoma
Mucoid carcinoma
Other types†
Molecular subtypes
Luminal A
Luminal B
Tumor size (T, cm)
Positive lymph node
TNM classification
N (%)
272 (42.2)
373 (57.8)
241 (37.4)
404 (62.6)
397 (61.6)
248 (38.4)
376 (58.3)
269 (41.7)
152 (23.6)
493 (76.4)
233 (36.1)
412 (63.9)
548 (85.0)
65 (10.0)
11 (1.7)
21 (3.3)
245 (38.0)
202 (31.3)
78 (12.1)
120 (18.6)
345 (53.5)
291 (45.1)
9 (1.4)
377 (58.5)
180 (27.9)
69 (10.7)
19 (2.9)
188 (29.1)
350 (54.4)
107 (16.5)
adenoid cystic carcinoma (1/21); micropapillary carcinoma (4/21); mixed carcinoma (8/21); neuroendocrine
carcinoma (2/21); cribriform carcinoma (3/21); apocrine
carcinoma (2/21); signet ring cell carcinoma (1/21).
lymph nodes’ status but avoiding ALND might
lead to breast cancer’s under-treatment, since
the accuracy of the status is a very important
factor in the implementation of systemic treatments. For those patients with FN SLN who
avoiding ALND, loco-regional disease control
may be discounted. Therefore, it is important to
minimize the FN rate of SLN if the patients
intent to avoid ALND. The present study reviewed the results of SLNB at Shandong Cancer
Hospital and Institute in China from January
2012 to December 2015. All suitable patients
underwent SLN biopsy, and then ALND was carried out. The SLN and non SLN simultaneous
removals were designed to evaluate the accuracy in prediction of the state of the axillary.
True positive (TP) is defined as sentinel lymph
node and axillary lymph node are all positive. In
this study, we compared the FN and TP in order
to determine the patients who are incline to be
FN and to gain a better benefit in the process of
surgical treatment.
The clinical and pathological data of 645 breast
cancer patients were collected in Shandong
Cancer Hospital and Institute in China from
January 2012 to December 2015 and retrospectively analyzed. Eligibility criteria were illustrated as follows: (1) all patients received the
ALND followed by SLNB; (2) no patients received
neoadjuvant therapy; (3) the axillary had no
previous surgical operation or radiotherapy; (4)
the immunohistochemical indicators included
ER, PR, HER2 and Ki-67. Breast cancer was
then classified based on the cancer staging of
American Joint Committee on Cancer (AJCC,
7th edition, 2010). The study was approved by
the Ethics Committee of Shandong Cancer
Hospital and Institute.
In this study, the streptavidin-peroxidase immunohistochemical method was used to detect
the expression of ER, PR, HER2 and Ki-67.
Cancer cells with nuclei positively stained by
ER, PR, and Ki-67 were considered to be positive, while HER2-positive was observed in the
cellular membrane or cytoplasm. ER- or
PR-positive were defined by at least 1% of
nuclei positively stained [9], while 20% of nuclei
positively stained by Ki-67 could be regarded
as high expression [10]. According to the guideline from the American Society of Clinical
Oncology and College of American Pathologists,
HER2 expression can be classified as HER2positive (score 3+), suspected HER2-positive
(score 2+) or HER2-negative (score 0 or 1+). For
Int J Clin Exp Med 2016;9(8):16703-16709
False negative in sentinel lymph node biopsy of breast cancer
Table 2. Comparison of clinicopathology between FN
Age at diagnosis
>49 years
≤49 years
ER status
PR status
HER2 status
Ki-67 status
Molecular subtype
Luminal A
Luminal B
SLN detection method
Methylene blue
99mTc-sulfur colloid
Combination method
Tumor size (T, cm)
Number of positive lymph nodes
18 222
21 161
17 192
22 191
23 306
16 77
24 299
15 84
11 38
28 345 11.529
17 115
22 268
11 169
14 176
8 30 28.079
10 107
11 134
18 142
15 161
24 222
27 146
11 176
1 61 15.175
those with suspected HER2-positive tumors,
fluorescence in situ hybridization should be
used to confirm their expression. According to
the Expert Consensus of the 2013 St Gallen
International Breast Cancer Conference [10],
breast cancer can be divided into four molecular subtypes on the basis of their molecular
markers. The typing criteria was as follow: (1)
luminal A: ER-positive, PR≥20% [11], HER2negative and Ki-67≤20%; (2) Luminal B (HER2negative): ER-positive, HER2-negative, PR≥20%
[11] or Ki-67>20%; (3) Luminal B (HER216705
positive): ER-positive and HER2-positive;
(4) HER2-enriched: ER-negative, PR-negative, HER2-positive; (5) TNBC: ER-negative, PR-negative, HER2-negative.
Methylene blue (Jiangsu Jichuan Pharmaceutical Co., Ltd., H32024827) or Carbon Nanoparticles Suspension Injection
(Chongqing Lummy pharmaceutical Limited by Share Ltd, H20073246) combined
with 99mTc-sulfur colloid were used to
search for SLN. 99mTc-sulfur colloid (0.51.0 mCi/0.5-2.0 ml) was subdermally
injected into the cutaneous projection of
the breast tumor 3-20 h before operation. Methylene blue (2 ml) or carbon
nanoparticles suspension (1 ml) was
injected to breast areola 15-30 min before operation. We used gamma-detecting probe to detect the SLN, and recorded the radiation intensity intraoperatively. Each radioactive lymph node with a
probe count >10% comparing with the
hottest node was removed as the SLN.
Statistical analysis
Data was analyzed using SPSS 17.0 software (SPSS Inc., Chicago, Illinois, USA).
According to the criteria of Louisville
University of SLNB technology, false negative (FN) rate = FN/(FN+TP); negative
predictive value = true negative/ALNnegative; accuracy rate = (TP+true negative)/ALN-positive; test was used to compare the difference between two groups.
Multivariate analysis was performed by
using Logistic regression model. All tests
were considered to be statistically significant when the p value was <0.05.
General results
Between January 2012 and December 2015, a
total of 645 patients underwent SLNB followed
by ALND were illustrated in Table 1. The median age of the patients was 49 (range 26-80)
years. Among the 645 patients, the median
number of SLN identified was 4 (range 1-12). A
positive SLN result was found in 391 patients
(60.6%), a positive SLN and with axillary node
metastasis was identified in 383 patients
(59.4%) and FN SLN was found in 39 patients
Int J Clin Exp Med 2016;9(8):16703-16709
False negative in sentinel lymph node biopsy of breast cancer
Table 3. A multivariate logistic regression model to analysis of SLN
Stage at diagnosis
Menopausal status
ER status
PR status
HER2 status
Ki-67 status
Molecular subtype
Tumor size
Number of positive lymph node
95% CI
0.977 0.899~1.063 0.591
0.985 0.950~1.020 0.395
0.124 0.026~0.580 0.008
1.052 0.235~4.711 0.948
3.703 0.788~17.399 0.009
1.009 0.975~1.043 0.623
2.000 0.477~8.387 0.343
1.561 0.928~2.626 0.093
0.009 0.100~0.718 0.009
Comparison of axillary lymph node
metastasis in different levels
In those FN SLN patients, there were
56.4% of positive lymph node were
occurred in Level I, 12.8% in Level II
and 5.1% in Level III. Positives lymph
nodes occurred in Level I and Level II
were in 23.1%. When SLN was negative, Level I and/or Level II harbored
metastases in 92.3% patients (Table
ER: estrogen receptor; PR: progesterone receptor; HER2: human epidermal growth factor receptor 2; SLN: Sentinel lymph nodes.
Table 4. Axillary lymph node status in breast
cancer patients with negative SLN
Level I
Level II
Level III
Case number (%)
22 (56.4%)
5 (12.8%)
2 (5.1%)
9 (23.1%)
1 (2.6%)
(9.2%). The number of patients with SLN-positive and ALN-negative was 8 (1.2%). True negative SLN was found in 215 patients (33.3%).
Negative predictive value was 96.4% (215/223).
Accuracy rate was 92.7% (494/598).
Correlation of FN SLN and TP SLN regarding
clinical pathological characteristics
A significant difference was observed in FN in
Table 2 for ER negative (P=0.003), PR negative
(P=0.02), HER2 positive (P=0.001), HER2enriched subtype (P=0.004), less than 3 positive lymph node (P=0.002). No significant difference was found between FN and TP regarding
age at diagnosis, menopause status, Ki-67 status and tumor size (all P>0.05). A multivariate
logistic regression model confirmed that ER
status (OR=0.124, P<0.05), HER2 status (OR=
3.703, P<0.05) and the numbers of positive
lymph nodes (OR=0.009, P<0.05) were all independent factors predicting FN results (Table
Sentinel lymph node biopsy has become an acceptable way of lymph
node status staging in axillary-nodenegative patients. Because ALND is potentially
associated with marked morbidity, Limb edema, numbness, activity limitation and some
other complications, some have questioned
whether ALND suitable for all breast cancer
patients. With the increasing use of SLNB, FN
SLN is a thorny problem to be faced. In many
areas of China, SLNB technology is not a widely
accepted method for several reasons such as
exiting FN, equipment condition backwardness.
According to the breast cancer treatment consensus, for those patients with negative SLN,
they may escape from radiotherapy. FN SLN
could be the source of future recurrence.
Previous studies have reported that the FN rate
of SLN was 4%-29% [12-16]. In this study, FN
rate was 9.2%, which approached the average
level compared with the majority of the reports.
The varied false negative rate of SLN may be
depending upon the surgeons’ proficiency and
detection method. In our research, the accurate rate in determining axillary lymph node status was 92.7%, which is close to Pargaonkar et
al. [17] reported.
In this study, comparing FN with TP, FN was
associated with ER and PR negative breast
cancer. Andersson et al. [18] also have reported a higher FN rate (28%) in hormone receptornegative patients. While Zabagno et al. [19]
have reported a lack of correlation between
ER/PR and FN rate. The different results may
be owing to the judgment standard of ER and
PR or ethnic difference. In the present study,
HER2-enriched is inclined to be FN. The reason
may be related to the aggression of cancer. The
cancer embolus blocked lymphatic that can
Int J Clin Exp Med 2016;9(8):16703-16709
False negative in sentinel lymph node biopsy of breast cancer
mislead the tracer normal drainage. Another
reason may be due to the inability of macrophage to uptake the tracer, preventing the tracer from entering into the lymphatic system.
as unskilled surgeons and poor equipment
In our study, the more positive axillary lymph
nodes were detected, the less possibility for
SLN appeared to be FN. This result was consistent with most of the previous research reports
[18, 20-22]. When the number of SLNs were 1,
2, 3 and 4, FN SLN rates were 30.5%, 23.1%,
14.3% and 4.5%, respectively. With the increasing number of SLN, the FN rate decreased.
Previous study reported that when the SLN was
more than 4, the diagnostic accuracy is significantly improved [23]. Our study showed that
when SLN was up to 5, there was no FN eventually. We found no relationship with injection
method, whatever methylene blue, 99mTc-sulfur colloid or in combination and this is consistent with Martin’s [22] report.
This study was supported in part by Shandong
Academy of Medical Sciences (2015-58).
According to the American College of Surgeons
Oncology Group (ACOSOG) Z0011 test [24],
based on the T1-2 stage breast cancer patients,
there were no significant differences on fiveyear survival of those patients no more than 2
positive SLN with or without ALND. While these
patients experienced breast conserving surgery and went through postoperative radiotherapy. Due to clinical benefit and feasibility, SLNB
replacement of ALND was becoming more popular in clinic [25]. Absolutely, it is important that
the FN rate should be reduced, especially for
those who have no opportunity to get postoperative radiotherapy. For those patients with
FN, we found that most of the positive node
located in Level I and Level II, and it is necessary to take axillary lymph nodes dissection of
Level I and Level II in order to reduce the cancer residual if the surgeon is unskilled or equipment condition is backward.
Reducing the FN rate is the backbone of SLNB
as a substitute operation, so we could omit axillary lymph node dissection. To achieve this
goal, we must assure to evaluate the SLN accurately. The present study suggested that FN
SLN was significantly related to ER, PR and
HER2 status, molecular subtypes. In spite of
negative SLN, the exploration of Level I and
Level II lymph node status may be a relatively
safe measure for those high-risk patients, considering the limited medical conditions, such
Disclosure of conflict of interest
Address correspondence to: Dr. Zhiyong Yu, Shandong Breast Disease Center, Shandong Cancer Hospital Affiliated to Shandong University, Jinan 250117,
Shandong, P. R. China. Tel: 0086-0531-67626960;
E-mail: [email protected]
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