Asian Pacific Journal of Cancer Prevention, Vol 14, 2013 2657
Frozen Section Analysis of Sentinel Lymph Nodes for Detection of Breast Cancer Micro Metastasis
Asian Pacific J Cancer Prev, 14 (4), 2657-2662
dilemma for many years and has romped havoc with
life of many patients. It is the leading cause of cancer
morbidity and mortality among women all over the world.
The reported incidence of reproductive age breast cancer
is highest globally (Bhurgri et al., 2007). In Karachi,
it annals for one thirds of female malignancies. This
actuality has established major concerns regarding the
clinical management of breast cancers. Axillary lymph
node metastasis is the most important prognostic factor in
breast cancer and therefore has major clinical implication
on its management (Fisher et al., 1983).
Sentinel lymph node (SLN) biopsy became standard
of care for clinically node negative breast cancer patients
Breast cancer has proffered as a serious public health
1Department of Histopathology, Liaquat National Hospital and Medical College, Karachi, 2Department of Medical Oncology, Sindh
Institute of Urology and Transplantation, 3Department of Pathology and Microbiology, Aga Khan University Hospital, Pakistan
*For correspondence: email@example.com
with clinically node negative breast cancer for diagnosis and also in order to determine the need for immediate
axillary clearance. Several large scale studies confirmed the diagnostic reliability of this method. However,
micrometastases are frequently missed on frozen sections. Recent studies showed that both disease free interval
and overall survival are significantly affected by the presence of micrometastatic disease. The aim of this study
was to determine the sensitivity and specificity of intraoperative frozen section analysis of sentinel lymph nodes
(SLNs) for the detection of breast cancer micrometastasis and to evaluate the status of non-sentinel lymph nodes
(non-SLNs) in those patients subjected to further axillary sampling. Materials and Methods: We performed
a retrospective study on 154 patients who underwent SLN biopsy from January 2008 till October 2011. The
SLNs were sectioned at 2 mm intervals and submitted entirely for frozen sections. Three levels of each section
submitted are examined and the results were compared with further levels on paraffin sections. Results: Overall
40% of patients (62/154) were found to be SLN positive on final (paraffin section) histology, out of which 44
demonstrated macrometastases (>2mm) and 18 micrometastases (<2mm). The overall sensitivity and specificity
of frozen section analysis of SLN for the detection of macrometastasis was found to be 100% while those for
micrometastasis were 33.3% and 100%, respectively. Moreover 20% of patients who had micrometastases in
SLN had positive non-SLNs on final histology. Conclusions: Frozen section analysis of SLNs lacks sufficient
accuracy to rule out micrometastasis by current protocols. Therefore these need to be revised in order to pick up
micrometastasis which appears to have clinical significance. We suggest that this can be achieved by examining
more step sections of blocks.
Keywords: Micrometastasis - sentinel lymph node biopsy - breast cancer - frozen section
Background: Intraoperative sentinel lymph node biopsy has now become the standard of care for patients
Accuracy of Frozen Section Analysis of Sentinel Lymph Nodes
for the Detection of Asian Breast Cancer Micrometastasis -
Experience from Pakistan
Atif Ali Hashmi1*, Naveen Faridi1, Amna Khurshid1, Hanna Naqvi1, Babar
Malik2, Faisal Riaz Malik3, Zubaida Fida1, Shafaq Mujtuba1
because it has significantly reduced the morbidity of breast
surgery (Giuliano et al., 1994; Veronesi et al., 1997).
This technique involves the identification of first node(s)
draining the tumor area by the introduction of a vital blue
dye or radio-labelled substance. SLNs are examined by
frozen section or imprint cytology and if they are positive
for malignancy, axillary lymph node dissection (ALND)
is carried out in same period of time. On the other hand
if they are negative for tumor, the probability of tumor
metastasis in non-sentinel lymph nodes (non-SLN) is very
low (Veronesi et al., 1999; Viale et al., 1999), so surgeons
can relinquish the ALND procedure. However limited
axillary sampling can be done if the index of suspicion is
The American Joint Committee on Cancer (Edge et
al., 2010) classified tumor deposits of less than 2 mm in
Atif Ali Hashmi et al
diameter in SLNs into micrometastasis and isolated tumor
cells (ITCs). Micrometastasis is defined as metastasis that
are larger than 0.2 mm in diameter but 2 mm or smaller,
denoted as lymph node positive (pN1mi), whereas Isolated
tumor cells are defined as tumor cell clusters that are more
than 0.2 mm in largest diameter and are denoted as lymph
node negative [pN0(i+)]. Tumor deposits which measure
more than 2 mm are referred as macrometastasis.
Although SLN biopsy has contributed to conspicuous
decrease in the overall morbidity of breast surgery,
however a consensus has not been reached regarding its
standardization. This is primarily because the clinical
significance of previously unrecognized micrometastasis
is still unclear. The sensitivity of frozen section of SLNs
in the detection of micrometastasis also varies from
institution to institution because it largely depends on the
method of analysis and the extent of sampling adopted.
The aim of this study is to determine the accuracy of
intraoperative frozen section analysis of SLNs for the
detection of breast cancer micrometastasis and to evaluate
the status of non-SLNs in those patients who are subjected
to further axillary sampling.
Materials and Methods
Asian Pacific Journal of Cancer Prevention, Vol 14, 2013 2658
154 patients who underwent breast surgery for clinically
node negative breast cancer from January 2008 till
October 2011. An approval from institutional ethical
review committee was obtained antecedent to conducting
the study. Informed consent from patients was obtained
prior to surgery. To perform SLN biopsy procedure,
lymphoscintigraphy was done. In this procedure 99mTc-
albumin nanocolloid was prepared and then injected in the
subareolar area of the patient. Scintigraphic imaging was
acquired using gamma camera within 5 minutes after the
injection. During the biopsy a gamma camera was used
to determine which nodes had absorbed the radionuclide
dye. These lymph nodes which may be one to several
in number were labelled as SLNs; they were dissected
and sent to histopathology laboratory for frozen section
analysis. The received SLNs were sectioned at an interval
of 2 mm and submitted entirely for frozen section. The
6-10 um thick sections were made at three levels from each
piece submitted and stained with hematoxylin and eosin
(H&E) stains. The frozen section results were reported as
negative or positive for metastasis. In all those cases where
the result of frozen section is positive for metastasis (either
macro or micrometastasis) complete ALND was carried
out at the same time. On the other hand when the result
of frozen section was negative, patients were subjected
to no further axillary sampling. After the frozen section
results were reported, all pieces were paraffin embedded
and one to three further levels were examined. One case
of micrometastasis was also confirmed by cytokeratin
(AE1/AE3) immunohistochemical stain. The results of
frozen and paraffin sections were both mentioned in the
final report. Furthermore histological type of tumor, extent
of invasion, tumor grade and non-sentinel axillary lymph
node status were also recorded.
We performed a retrospective observational study on
34% of patients had modified radical mastectomy, while
the rest underwent breast conservation surgeries including,
lumpectomy with or without axillary dissection and simple
mastectomy (Figure 1). The breast cancer incidence was
most common age group between 30-50 years (Figure 2).
This also coincides with the national data as discussed
Most of the tumors were in stage T2 range (Figure 3).
Infiltrating ductal carcinoma comprised the most common
subtype of the tumor accounting for 80% of the cases
(Table 1) and tumors were grade II (Figure 4). The number
of SLNs per patient ranged from 1 to 5 with a mean of 2.3.
Overall 40.3% of cases (62/154) of SLNs were positive
Out of 154 patients who were included in the study,
Figure 1. Type of Surgical Specimens
Figure 2. Age Distribution
Figure 3. Tumor Size Distribution
Figure 4. Tumor Grades
Asian Pacific Journal of Cancer Prevention, Vol 14, 2013 2659
Frozen Section Analysis of Sentinel Lymph Nodes for Detection of Breast Cancer Micro Metastasis
on final histology out of which 44 were macrometastasis
and 18 were micrometastasis.
Table 2 compares the results of frozen sections and
corresponding results of paraffin sections. A total of 154
cases of SLNs were examined, out of which 50 were
positive on frozen section. There were 12 cases in which
frozen section results were discordant with the final
paraffin section diagnosis and all these cases were that of
Table 3 further emphasizes the results of SLN biopsy
with breakdown of positive results into macrometastasis
and micrometastasis. Its shows that all 44 cases of
macrometastasis were correctly identified on frozen
section, on the other hand in cases of micrometastasis 6 out
of 18 cases were correctly diagnosed on frozen section and
12 cases which were labelled negative at time of frozen
section, the diagnosis was changed with paraffin section
results giving a false negative rate of 66.7%.
Table 3 summarizes the overall sensitivity and
specificity of frozen section analysis of SLNs. The
overall sensitivity is 80.6% with 100% specificity. For
macrometastasis detection the sensitivity was 100%,
however in the cases of micrometastasis the sensitivity is
only 33.3% with 100% specificity.
Out of total 154 patients, 108 patients underwent
further axillary dissection after SLN biopsy. Table 4
shows the frequency of non-SLN metastasis in all these
patients. All 44 patients who had positive SLN with
macrometastasis had complete axillary dissection and
the nodes thus recovered were designated as non-SLNs.
Out of these 44 cases of macrometastasis, 19 (43.2%)
cases had positive non-SLNs. Out of total 18 patients
who had a final diagnosis of micrometastasis in SLNs, 10
had further axillary dissection/sampling, out of which 2
(20%) had positive non-SLNs. Finally out of 92 patients
who had negative SLNs, 54 patients underwent further
axillary sampling, out of which 5 (9.3%) were positive
Table 6 shows the frequency of lymphovascular
invasion which is considered as a marker of nodal
metastasis in these patients. In those patients who had
positive SLNs with macrometastasis and micrometastasis,
13 (29.5%) and 2 (20%) cases had lymphovascular
invasion respectively. Even in patients with negative
SLNs 19 (17.6%) caes were positive for lymphovascular
Breast cancer is the most frequent cancer of women
in Karachi, accounting for one third of cancers in women.
The tumor burden of breast cancer in our population is
highest in Asia (Bhurgri et al., 2006).
SLN biopsy is an area of extensive research in the
Table 1. Types of Tumor
Tumor type n %
Infiltrating ductal carcinoma
Infiltrating lobular carcinoma
Infiltrating carcinoma(cannot be specified) 12
124 80.5 80.5
Total 154 100 100
Table 2. Sentinel Lymph Nodes, Frozen Section
Diagnosis vs. Paraffin Section Diagnosis
Paraffin section diagnosis
Frozen section diagnosis
Total n 62 92 154
Table 3. Sentinel Lymph Nodes, Frozen Section
Diagnosis vs. Paraffin Section Diagnosis with
Comparison of Macrometastasis and Micrometastasis
Frozen Section Positive
Frozen Section Positive
Negative Sentinel Lymph Nodes
Frozen Section Negative
Total Frozen Section Positive
Table 4. Sensitivity and Specificity of Frozen Section
Biopsy of Sentinel Lymph Nodes
Variable Sensitivity Specificity
Frozen section of sentinel lymph node biopsy 80.60%
Table 5. Sentinel Lymph Nodes vs. Axillary (non-
sentinel) Lymph Nodes
Axillary (non-sentinel) lymph nodes Total
Sentinel Lymph Nodes
Macrometastasis 19 (43.2%)
Negative S.L.Nodes 5 (9.3%)
Total 26 (24.1%) 82 (75.9%) 108
Table 6. Sentinel Lymph Nodes vs. Lymphovascular
Present Not Present
Sentinel Lymph Nodes
13 (29.5%) 31 (70.5%)
4 (7.4%) 50 (92.6%)
Total 19 (17.6%) 89 (82.4%) 108
Atif Ali Hashmi et al
staging and management of breast cancer. By reducing
the number of nodes to be examined, more exhaustive
histopathological approach for examining SLNs become
possible. Intraoperative analysis of SLNs can be done
by imprint cytology or frozen sections. Frozen section
evaluation is slightly superior to imprint cytology.
Numerous studies evaluated the accuracy of intraoperative
frozen section and the sensitivity depends on the method
of examination adopted. A meta-analysis reported the
sensitivity of intraoperative frozen section, ranging
from 57-74% (Layfield et al., 2011). The detection rate
for micrometastasis in other studies is reported to range
from 9-46% (Dowlatshahi et al., 1999; Tille et al., 2009),
whereas in our study the overall sensitivity was 80.6% and
for micrometastasis the sensitivity was found to be 33.3%.
SLN is a very labor intensive technique but still
controversies exist around its protocol. This is primarily
because current data from large scale clinical trials is still
insufficient to answer two central questions. First, what
is the frequency of non-SLN metastasis in the absence
of SLN involvement and long term axillary recurrence,
and second, the clinical significance of micrometastasis
and ITCs which are frequently missed on frozen sections.
Regarding first, multiple studies evaluated this issue and
reported the frequency of non-SLN metastasis ranging
from 5-13% (Giuliano et al., 1994; Krag et al., 1998;
Turner et al., 1999; Weaver et al., 2000) with negative
SLNs. O’Hea et al. (1998) in a study noted involvement of
non-SLNs in 5 patients with a frequency of 13%. Giuliano
et al. (1994) similarly found non-SLN metastasis in 11%
of cases in a study of 174 patients. In our study 5 out of 54
patients who had negative SLNs demonstrated non-SLN
metastasis with a frequency of 9.3%.
The most difficult question to answer which posed
frequent problems for breast surgeons, pathologists and
researchers is to determine the clinical significance of
micrometastasis. This is because most of the studies to date
are hampered due to lack of long term follow up and short
sample size in order to clearly define the clinical relevance
of micrometastasis and isolated tumor cells. Cohort studies
reported the survival rates in patients with micrometastasis
or isolated tumor cells and found no reduced recurrence
free survival (Liang et al., 2001; Chagpar et al., 2005; Fan
et al., 2005; Soni et al., 2005; Imoto, 2006; Nagashima et
al., 2006). On the other hand two studies reported a higher
recurrence rate for patients with micrometastasis (Rydén
et al., 2007; Cox et al., 2008) They also found additional
metastasis in non-SLNs.
It is well established that the need for complete ALND
in T1 and T2, clinically node negative breast cancer
depends on the results of sentinel lymph node biopsy,
however the indications are evolving (Sanuki et al., 2013).
Although there is no question on the performance of
complete ALND if micrometastasis or macrometastasis
are found in three or more nodes, however the need for a
complete ALND in patients with a positive SLN showing
micrometastases or macrometastases in less than three
nodes has been argued (Carlson et al., 2011). The SLN is
the sole tumor-bearing node in up to 60% of cases overall,
and in almost 90% of patients harbor only micrometastatic
disease. These observations have led to speculation that
Asian Pacific Journal of Cancer Prevention, Vol 14, 20132660
complete ALND may not be necessary in selected patients
with a positive SLN in less than three nodes because the
need for systemic therapy is established and the risk of
an axillary recurrence appears to be low.
The American College of Surgeons Oncology Group
(ACOSOG Z-0011) trial was designed to address the need
for complete ALND for patients with T1 or T2 tumors
that were clinically node negative and had less than three
positive SLNs (Giuliano et al., 2010; 2011); all patients
were treated with radiation to the breast. The five-year
overall survival was similar whether women were treated
with SLND plus ALND or with SLN biopsy alone (91.9
versus 92.5 percent, respectively). Recurrence rates in
the ipsilateral axilla were similar between the two arms
with four recurrences (0.9%) in the SLN biopsy alone arm
compared with two recurrences (0.5%) in the ALND arm.
The International Breast Cancer Study Group trial
23-01 (IBCSG 23-01) randomized patients with SLN
micrometastases (<2 mm) and primary tumors <5 cm
in size to either completion ALND or SLN biopsy alone
(Galimberti V;International Breast Cancer Study Group
Trial 23-01).The study included 931 patients. With a
median follow-up of 49 months, there was no significant
difference in disease free survival rate for patients treated
with an ALND compared with those treated with a SLN
biopsy alone (87 versus 92%). There was no significant
difference in overall survival rate for patients treated with
an ALND compared with those treated with a SLN biopsy
(97.6 versus 98.0%).
In 2013, we are still debating and trying to understand
the clinical significance of micrometastasis in breast
SLNS. In an analysis of population-based data from the
National Cancer Institute’s Surveillance, Epidemiology,
and End Results (SEER) national cancer database showed
that the presence of micrometastasis in lymph nodes is
associated with an overall decrease in survival at 10 years
of 1% for T1, 6% for T2, and 2% for T3 breast cancers
when compared to patients with negative axillary nodes
(Chen et al., 2007). As new more and more studies are
coming up regarding prognostic value of micrometastasis,
our study also showed non-SLN involvement in 2 cases
(20%) with micrometastatic disease in SLN and 5 cases
(9.3%) with negative SLNs. Therefore we suggest that
more intensified pathological assessment of SLNS need
to be done.
In our study we have not performed molecular
studies on SLNs to detect micrometastasis/ITCs due to
unavailability of this facility at our setup. Considering the
existing controversy about significance of micrometastasis,
reverse transcriptase – polymerase chain reaction (RT –
PCR) which having been studied for several years is
still not recommended for detecting micrometastasis/
ITCs in axillary lymph nodes. Moreover in our study,
immunohistochemical stains were not performed on SLNs
in every case, which may be the reason why ITCs were
not detected in any case.
There is no standard agreement regarding how to
examine SLNs and institutions have developed their
own in-house protocols to evaluate SLNs. AJCC does not
specify a grossing protocol for SLN biopsy. According to
College of American Pathologists and American Society
Asian Pacific Journal of Cancer Prevention, Vol 14, 2013 2661
Frozen Section Analysis of Sentinel Lymph Nodes for Detection of Breast Cancer Micro Metastasis
of Clinical Oncology guidelines, SLNs should be sliced
at an interval of 2 mm and one level should be examined
from each block. This protocol is particularly designed
for the detection of macrometastasis. However they stated
that, the detection of micrometastasis can be enhanced by
examining more step sections of the block.
Although large scale clinical trials to determine the
clinical significance of occult metastasis are underway
but it seems likely from the results of a few recent
studies that micrometastasis do appear to have clinical
significance and impact on long term survival. Detection
of micrometastasis in SLN is a grave challenge but
hypothetically speaking its detection can be enhanced by
examining whole SLN at predetermined intervals.
In conclusion, frozen section analysis of SLNs lacks
sufficient accuracy to rule out micrometastasis by current
protocols which include examining sections at an interval
of 2 mm. Presence of micrometastasis in SLNs appears to
increase the likelihood of positive non-SLNs and perhaps
the risk of axillary recurrence and long term disease free
survival. Examining more step sections or perhaps whole
node at evenly spaced levels (200- to 500-um) can increase
the sentisitivity of frozen section for the detection of
micrometastasis. However more large scale prospective
studies are needed to prove the clinical significance of
micrometastasis, so that a standard protocol can be devised
for SLN evaluation.
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