252 Med Arh.

2013 Aug; 67(4): 252-255 ORIGINAL PAPER

Diagnostic Accuracy of Sentinel Lymph Node Biopsy in Axillary Lymph Nodes at the Early Stages of Breast Cancer
DOI: 10.5455/medarh.2013.67.252-255
Med Arh. 2013 Aug; 67(4): 252-255
Received: May 28th 2013 | Accepted: July 25th 2013
CONFLICT OF INTEREST: NONE DECLARED
ORIGINAL PAPER
Diagnostic Accuracy of Sentinel Lymph Node
Biopsy in Axillary Lymph Nodes at the Early
Stages of Breast Cancer
Sadat Pusina
Clinic of Oncology and Glandular Surgery, Clinical Center of Sarajevo University, Bosnia and Herzegovina
I
ntroduction: For almost 100 years, standard procedure for evaluation of axillary lymph node
status has been axillary nodes dissection (ALDN)dissection of 1
st
, 2
nd
or possible 3
rd
level of
axilla. Use of less invasive evaluation methods of axillary node pathologically (PH) status of
non-invasive breast carcinoma has been started before about 30 year and that new method has
been named sentinel lymph node biopsy (SLNB). Objective: Primary objective of study is to es-
tablish specifcity, sensitivity, positive and negative predictive value of SLNB method comparing
to presents of malignant changes of axillary sentinel lymph node and to establish true indication
for ALDN. Patients: Study included 50 female patients, aged between 18-75, at Clinic for Glan-
dular and Oncological Surgery, Clinical Center University of Sarajevo (CCUS), with non-invasive
breast carcinoma, in the period from January 2008-January 2011, which fulfll established criteria.
Material and methods: Te study is of retrospective-prospective, clinical-manipulative and
descriptive-analytic character. Sample consisted of patients of Clinic for Glandular and Onco-
logical Surgery with diagnosed breast carcinoma, at T1 and T2 stage, with adequate preoperative
preparation. Preoperative imaging with injection of radioactive isotope Tc99m albumin-colloid
is done at the Clinic for Nuclear Medicine CCUS. Intraoperative PH examination of SLN node
(or nodes) by frozen-section and hematoxylin-eosin staining and postoperative PH examination
of lymph nodes after ALND was done at the Institute for Clinical Pathology and Cytology CCUS.
Intraoperative identifcation of SLN is done with manual gamma probe. After the SLNB, all the
patients underwent immediately appropriate breast carcinoma surgeries followed with dissection
of 1
st
and 2
nd
level of axilla on the Clinic for oncology and glandular surgery of CCUS. Results:
Statistic data evaluation was done by statistical program Med Calc for Windows, version 12.2.1.0
(MedCalc Software Mariakerke, Belgium). In the part of descriptive statistics all results are shown
in table manner: mean, 95% CI for average value, standard deviation, median values, 95% CI for
median value, maximal value, 25-75 percentiles, evaluation of normal distribution by DAgostino-
Pearson test, Chi square test for evaluation of diferences in frequencies between subgroups. For
evaluations of specifcity and sensitivity of results were applied 2x2 tables and following equations:
sensitivity=TP/TP+LN, specifcity=TN/P+TN, overall accuracy = TP+TN/N, positive predictive
value= TP/TP+LP, negative predictive value = TN/LN+TN. Defned signifcance level was p<0.05.
Conclusions: Results of sensitivity (68%), specifcity (98%), positive (67%) and negative predictive
value (96%) and overall accuracy of method (98%) are comparable and compatible with results from
oncological breast cancer centers and allow introducing of SLNB in routine surgical practice in our
clinical practice as the alternative for ALND for T1 and T2 breast carcinoma. It also contributes to
better co-ordination between specialist of nuclear medicine, surgeon and pathologist. Key words:
breast carcinoma, radioactive isotope, sentinel lymph node biopsy
Corresponding author: Sadat Pusina, MD. E-mail:sadat@gmail.com
1. INTRODUCTION
Standard procedure for the assess-
ment of axillary lymph nodes for more
than 100 years was axillary lymph node
dissection (ALND)which involves dis-
section of 1
st
, 2
nd
and 3
rd
levels of axilla,
associated with signifcant morbidity
including pain, numbness and tingling,
seroma, infection, limited movements
of the shoulder and lymphedema of the
upper arm.
Tanks to the work of Morton et al.
with melanoma of the skin, as well as
the fact that the skin and breast tissue
have common embryonic origin, there
was the idea of applying a less invasive
diagnostic methods for the assessment
of tumor status of axillaaxillary sen-
tinel lymph node biopsy (SLNB) (1). By
terminology, axillary sentinel lymph
node is the frst node that stands in the
way of the lymphatic drainage of the
primary tumor and that in a large per-
centage represents a tumor status of the
remaining axillary lymph nodes basin.
About 85% of lymphatic drainage
from any quadrant of the breast drains
its lymph to axillary lymph nodes,
so that axillary SLN with high preci-
sion represents the status of the re-
maining lymph nodes in the axilla (2).
Sentinel lymph node (one or more)
should a) be the frst lymph node in
lymph drainage path from localization
of the primary tumor to the regional
lymph basin, b) that it can successfully
be marked with a radioactive isotope
253 Med Arh. 2013 Aug; 67(4): 252-255 ORIGINAL PAPER
Diagnostic Accuracy of Sentinel Lymph Node Biopsy in Axillary Lymph Nodes at the Early Stages of Breast Cancer
or dye and c) that it can be successfully
identifed.
Kreigh et al. (1993) were the frst
to present data on successful applica-
tion of unfltered Tc99 in breast can-
cer and identifcation of sentinel lymph
nodes in 18 of 22 patients using a man-
ual gamma probe that was followed by
numerous other studies (Giliano et al.,
Albertini and al., Veronesi et al., Imoto
et al., Motomura et al.) that used ei-
ther dye or radioactive isotope label-
ing as a means for marking axillary
SLN which had a percentage of iden-
tifying over 90% with the percentage
of false-negative results below 10% (3).
However, SLN biopsy is a relatively new
method that has not yet been standard-
ized and that requires clearly defned
and precise collaboration between nu-
clear medicine specialists, pathologists
and surgeon.
Terefore, all the authors in the be-
ginning of application of SLN biopsy
validate the results with complete axil-
lary lymph node dissection (or axillary
backup). Until now are made 69 clini-
cal studies as well as fve multicenter
study in which the results of SLN bi-
opsy were evaluated with ALND (4).
According to estimates American Can-
cer Society in the 2011/2012 year, at the
United States discovered 230480 new
cases of invasive breast cancer with
an additional 57650 women who had
been diagnosed with breast cancer in
situ (5).
Although all present radiological
techniques can defne the parameter
T and M parameter in patients with
newly diagnosed breast cancer, their
diagnostic value is unacceptably low
and too expensive for the prediction of
the parameter N in patients with neg-
ative clinical fnding. Mammography
screening procedure has resulted in
the detection of breast cancer at early
stage where the probability of the pres-
ence of axillary metastases is between
20-40% (T1a-c) and ALND is routinely
carried out in these patients as part of
the staging, regardless of clinically neg-
ative axilla (6).
ALND is associated with a high
incidence of early and late postop-
erative complications so that raises
the question of justifcation for rou-
tine axillary lymph node dissection
in all patients with breast cancer (7).
Detailed histological evaluation of 15 to
20 lymph nodes is practically impossible
during standard pathological analysis.
On other hand, focusing on only one or
a few sentinel lymph nodes in the course
of extensive histological analysis im-
proves the accuracy of the histopatho-
logical axillary lymph nodes staging (8).
Randomized clinical trials have con-
firmed that avoiding axillary dis-
section in breast cancer with nega-
tive sentinel lymph nodes can main-
tain the current parameters for loco-
regional recurrence and overall sur-
vival, while reducing the percentage
of postoperative morbidity (9,10,11).
Terefore, the radioactive guided bi-
opsy of sentinel lymph node can be con-
sidered a new, minimally invasive stan-
dard axillary surgery in patients with
early-stage breast cancer.
2. GOAL
Te goal was to establish specifcity,
sensitivity, positive and negative predic-
tive value of SNLB method in relation
to the presence of malignant changes in
axillary sentinel lymph node and to de-
termine the actual need for implemen-
tation of ALND.
3. PATIENTS AND METHODS
3.1. Patients
Te study included 50 female pa-
tients at the Clinic of Glandular and
Oncological surgery CCU Sarajevo,
with an initial breast cancer, aged 18-75
years in the period from January 2008
to January 2011, and which fulflled the
predefned criteria.
3.2. Methods
Te study was of retrospective-pro-
spective clinical manipulative and de-
scriptive-analytical character. Te sam-
ple consisted of patients who were ad-
mitted to the Clinic of Oncology and
Glandular surgery with a di-
agnosis of breast cancer, at
stage T1 and T2, which have
been subjected to appropri-
ate preoperative preparation.
Preoperative injection of ra-
dio-active isotope Tc99 m al-
bumin-nanocolloid was car-
ried out at the Clinic of Nu-
clear Medicine CCUS, multi-
ple, subcutaneous, above tu-
mor at a dose of 0.2 ml, 640 mikroCi. In-
traoperative SLN identifcation is done
using manual gamma probe with ap-
propriate types of surgical breast can-
cer surgery and dissection of 1
st
and 2
nd

level of axillary lymph nodes performed
at the Clinic of Oncology and Glandu-
lar Surgery CCUS. PH treatment of in-
traoperative dissected SLN was carried
out at the Institute of Clinical Pathol-
ogy and Cytology CCUS according the
corresponding protocol.
Statistical analyzes were performed
in the statistical program Med Calc
for Windows, version 12.2.1.0. (Med-
Calc Software, Mariakerke, Belgium).
In the part relating to the descriptive
statistics all of the results are presented
in tables by: the mean value (arithme-
tic mean), 95% CI for the mean, stan-
dard deviation, median, 95% CI for the
median value, minimum value, maxi-
mum value, 25-75 percentiles, estimate
of normal distribution by DAgostino-
Pearson test, chi-square test, 2x2 tables
and formulas for evaluation of the sen-
sitivity, specifcity, PPV, NPV, and ac-
curacy. Values that is obtained with the
value of p <0.05 was accepted as statis-
tically signifcant. Te results of all an-
alyzes performed are presented in ta-
bles and charts.
4. RESULTS
Te study included 50 patients who
met criteria for inclusion in the study,
the average age of the patients was
51.3210.5 years, with the youngest at
age of 30 and the oldest at the age of 74
years. Analysis of tumor size showed
that the patients had an average tu-
mor size of 1.780.84 cm, with a 95%
confdence interval (95% CI) of 1.482
to 2.079 cm.
Most tumors were larger than 1.5
cm in a total of 24 (48%). Te largest re-
corded tumor size in the study was 4.0
4

<0.05 was accepted as statistically significant. The results of all analyzes performed are
presented in tables and charts.


4. RESULTS

The study included 50 patients who met criteria for inclusion in the study, the average
age of the patient's was 51.3210.5 years, with the youngest at age of 30 and the oldest at the
age of 74 years. Analysis of tumor size showed that the patients had an average tumor size of
1.780.84 cm, with a 95% confidence interval (95% CI) of 1.482 to 2.079 cm.
Figure 1. Tumor size (cm)

Most tumors were larger than 1.5 cm in a total of 24 (48%). The largest recorded
tumor size in the study was 4.0 cm and the smallest 0.2 cm. Intraoperative identification of
SLN (one or more) by gamma probe was performed in all patients as a condition for inclusion
of the patients into the study.
Most of the patients had undergone qudrantectomy (n = 21, 42%), and hemi
mastectomy (n = 14, 28%), mastectomy (n = 7, 14%), and finally bisegmenctetomy (n = 4,
8%) and segmentectomy (n = 4, 8%).
The histopathological analysis revealed that the most common cancers were ductal (n
= 27, 54%, p = 0.0184), and lobular (n = 12, 24%) followed by other types (n = 11, 22%).
Under group of other group most cancer was of tubulo-lobular (n = 4), and tubular (n = 3)
with one apocrine, mucinous, neuroendocrine and papillary. (Table 1)
Table 1. Histological types of the cancer
Cancer type n %

p
Ductal 27 54 0.0184
Lobular 12 24
Other 11 22
Total 50 100

All patients (n=50) underwent histopathological analysis of sentinel lymph nodes and
axillary lymph node involvement. On average was sent to analysis1.98 0.742 sentinel lymph
nodes, and 8.86 1.906 was the average number of lymph nodes after complete ALND.

0 1 2 3 4
Diametar tumora (cm) Tumor diemeter (cm)
Figure 1. Measuring of tumor size (in cm)
254 Med Arh. 2013 Aug; 67(4): 252-255 ORIGINAL PAPER
Diagnostic Accuracy of Sentinel Lymph Node Biopsy in Axillary Lymph Nodes at the Early Stages of Breast Cancer
cm and the smallest 0.2 cm. Intraopera-
tive identifcation of SLN (one or more)
by gamma probe was performed in all
patients as a condition for inclusion of
the patients into the study.
Most of the patients had undergone
qudrantectomy (n=21, 42%), and hemi
mastectomy (n=14, 28%), mastectomy
(n=7, 14%), and finally bisegmencte-
tomy (n=4, 8%) and segmentectomy
(n=4, 8%).
Te histopathological analysis re-
vealed that the most common cancers
were ductal (n=27, 54%, p=0.0184), and
lobular (n=12, 24%) followed by other
types (n=11, 22%). Under group of other
group most cancer was of tubulo-lob-
ular (n=4), and tubular (n=3) with one
apocrine, mucinous, neuroendocrine
and papillary (Table 1).
Cancer type n %
p
Ductal 27 54 0.0184
Lobular 12 24
Other 11 22
Total 50 100
Table 1. Histological types of the cancer
All patients (n=50) underwent his-
topathological analysis of sentinel
lymph nodes and axillary lymph node
involvement. On average was sent to
analysis1.98 0.742 sentinel lymph
nodes, and 8.86 1.906 was the aver-
age number of lymph nodes after com-
plete ALND.
Number of
SLN
Number of
axillary LN
after
ALND
N 50 50
Mean 1.980 8.860
95% CI 1.769-2.191 8.318-9.402
SD 0.7420 1.9061
Median 2.000 9.000
95% CI 2.000-2.000 8.000-9.000
Minimum 1.000 6.000
Maximum 4.000 15.000
Table 2. Lymph nodes analysis
TNM (TNM Classifcation of Ma-
lignant tumor) classifcation showed
that most patients with either with can-
cer in stage T1 (n=31, 62%, p= 0.0339),
and somewhat less in stage T2 (n=11,
22%) and the least number at the stage
Tcis (n=8, 16%). AJCC (American
Joint Committee of Can-
cer) classification showed
that most patients with any
stage of cancer was in Ia
stage (n=26, 52%, p=0.0661),
in stage Ib (n=15, 30%) and
in the stage 0 (n=5, 10%) with
the least number in the stage
IIa (n=4, 8%).
Figure 2 shows that the
average number of SLN in
the total sample was approx-
imately 2 (1.980.7) and
ranged from 1-4. In patients
with subsequent positive
PH fndings the number of
SLN was slightly higher and
ranged from 2-3, as com-
pared to those with nega-
tive PH fndings and ranged
from 1-4.
Te analysis of method sensitivity
and specifcity was done based on the
following data, positive or negative re-
sults of analysis of sentinel lymph nodes
and on the basis of positive or negative
fndings of axillary lymph nodes at the
same patient. In 46 patients there was a
negative result in sentinel lymph nodes
as well as in the axillary lymph nodes
and these fndings were classifed as
true negative (TN), in two patients
there was a positive fnding in the sen-
tinel lymph node and positive fndings
in lymph node and these was classifed
as a true positive (TP), in one patient
there was a positive fnding of sentinel
lymph node while the axillary lymph
node was negative so it is classifed as a
false positive result (FP), and fnally in
one patient the sentinel lymph nodes
were negative, while axillary lymph
nodes were found positive so this fnd-
ing is classifed as a false negative (FN)
fndings. (Table 3)
Based on the above analysis we ob-
tained sensitivity of 67%, specificity
98%, PPV of 67%, NPV of 96% and di-
agnostic accuracy of 98%.
5. DISCUSSION
Te hypothesis that one or more
sentinel lymph node receives most lym-
phatic drainage from the primary breast
tumor and axillary lymph node dissec-
tion can be avoided if the sentinel lymph
node is negative is logical, intuitive and
represents a new standard in the treat-
ment of early-stage breast cancer.
However, SLN biopsy is a rela-
tively new surgical technique that
has its own learning curve, which
i s a highly multidi scipl i nary and
which has not yet been standardized.
Te biggest dilemma regarding the use
of SLN biopsy method is the impact
on overall survival of patients and the
percentage of local axillary recurrence
compared to ALND. Results of several
randomized controlled trials in clini-
cally negative patients showed no difer-
ence in overall survival and local recur-
rence in patients who underwent SLNB
method only and those patients who
underwent simultaneous and SLNB and
ALND (9, 10, 11, 12, 13).
Diferent types of radioactive col-
loids are used when performing SLN
biopsy, diferent particle carriers size.
Using radio colloid particle size be-
tween 100 and 200 nm is a compro-
mise between fast lymphatic drainage
and optimum retention in the sentinel
lymph node.
Te percentage of sentinel lymph
node identifcation of 90-95% and the
percentage of false-negative results of
no more than 5-10% should be the tar-
get during the validation of the method
(9, 14, 15).
Te average number of SLN per pa-
tient was two lymph nodes, while biopsy
of more than 4 lymph nodes is not rec-
ommended due to the risk of develop-
5

Table 2. Lymph nodes analysis
Number of
SLN
Number of
axillary LN
after
ALND
N 50 50
Mean 1.980 8.860
95% CI 1.769 - 2.191 8.318 - 9.402
SD 0.7420 1.9061
Median 2.000 9.000
95% CI 2.000 - 2.000 8.000 - 9.000
Minimum 1.000 6.000
Maximum 4.000 15.000

TNM (TNM Classification of Malignant tumor) classification showed that most
patients with either with cancer in stage T1 (n=31, 62%, p= 0.0339), and somewhat less in
stage T2 (n=11, 22%) and the least number at the stage Tcis (n=8, 16%). AJCC (American
Joint Committee of Cancer) classification showed that most patients with any stage of cancer
was in Ia stage (n=26, 52%, p=0.0661), in stage Ib (n=15, 30%) and in the stage 0 (n=5, 10%)
with the least number in the stage IIa (n=4, 8%).




Figure 2. Average number of sentinel lymph nodes (SLN)
Figure 2 shows that the average number of SLN in the total sample was approximately
2 (1.980.7) and ranged from 1-4. In patients with subsequent positive PH findings the
number of SLN was slightly higher and ranged from 2-3, as compared to those with negative
PH findings and ranged from 1-4.

1,96 2,5 1,98
0
0,5
1
1,5
2
2,5
3
3,5
Number of SLN
Negative
Positive
Total
Figure 2. Average number of sentinel lymph nodes (SLN)
Results of axilla fndings
Meta
confrmed
Negative Total
SLNB
results
Positive TP 2 FP 1 TP+FP 3
Negative FN 1 TN 46 FN+TN 47
Total TP+FN 3 FP+TN 47 N 50
Table 3. Analysis of sensitivity and specifcity
255 Med Arh. 2013 Aug; 67(4): 252-255 ORIGINAL PAPER
Diagnostic Accuracy of Sentinel Lymph Node Biopsy in Axillary Lymph Nodes at the Early Stages of Breast Cancer
ing additional morbidity without addi-
tional benefts for the patient.
Recommendation of the American
Cancer Society Organization (ASCO) is
20-30 procedures per surgeon to check
the results of SLN biopsy with ALND,
although some papers indicate that a
smaller number of cases may be suf-
fcient (9).
After the ex tempore analysis
(FS) is negative sentinel lymph node
(or nodes) are routinely further exam-
ined by hematoxylin & eosin technique
(H&E) as a control ex tempore analy-
sis which is the standard practice of all
involved in SLNB. If the H&E technique
found negative nodes, remaining sen-
tinel lymph node can be further ana-
lyzed by immuno-histochemical meth-
ods for cytokeratin (IHC), which is not
yet standard practice of all centers that
deal with the treatment of breast cancer.
Results of studies of PH SLN analy-
sis shows that in about 10-20% of cases
when IHC is used for cytokeratin are
found micro metastases that are not
registered in the examination of senti-
nel lymph nodes by H&E technique (16).
In connection with the above is the
issue of treatment of micro metasta-
sis (<0.2 mm), their classifcation and
determination of appropriate stages of
breast cancer and the impact on the re-
currence and overall patient survival.
Primary non-detected metastases are
having prognostic and statistical sig-
nifcance associated with 10-15 % of
the deterioration in terms of overall
survival (17).
In general, monitoring of patients
after SLN biopsy was done during the
whole life. Clinical studies have multi-
year follow-up of patients after SLNB
and showed that the percentage of over-
all survival and disease-free period was
high (90.3 to 94.8% for overall survival
and 81.5 to 87.6% for disease-free pe-
riod) and was not signifcantly difer-
ent compared to ALND (13, 15)
6. CONCLUSION
Te obtained values of sensitivity,
specifcity, PPV, NPV, and accuracy of
the this method are compatible and
comparable with the results of the lead-
ing cancer centers that deal with breast
cancer surgery and allow the introduc-
tion of SLN biopsy method in every-
day surgical application at the Clinic of
Oncology and glandular surgery CCU
Sarajevo as a substitute for ALND in
case of T1 and T2 stage breast cancer,
with better co-ordination of multidis-
ciplinary team of CCUS consisting of:
surgeon, pathologist and nuclear med-
icine specialists.
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