Journal of Cancer Therapy, 2012, 3, 712-717 Published Online October 2012 (
The Size of Metastasis in the Sentinel Node Is a Predictor
of Additional Non-Sentinel Node Positivity
Todd A. Baker1, Nitin Wadhwani2, Prabha Rajan2, Sharfi Sarker1, Gerard Aranha1, Margo Shoup1,
Holly Mattix-Kramer3, Constantine Godellas1*
1Department of Surgery, Stritch School of Medicine, Loyola University Chicago, Maywood, USA; 2Department of Pathology, Stritch
School of Medicine, Loyola University Chicago, Maywood, USA; 3Department of Preventative Medicine and Epidemiology, Stritch
School of Medicine, Loyola University Chicago, Maywood, USA.
Email: *
Received August 29th, 2012; revised September 30th, 2012; accepted October 8th, 2012
Background: The need for axillary lymph node dissection (ALND) when sentinel lymph nodes (SLN) contain micro-
metastasis is controversial. The purpose of this study was to determine if the size of tumor in the SLN corresponds with
additional positive non-sentinel lymph nodes (non-SLN) in pT1 breast cancer. Methods: This retrospective review of
483 patients with pT1 breast cancer identified 96 patients with tumor positive SLN biopsies between June 1999 and
February 2010. The size of SLN metastasis and the number of tumor positive non-SLN were recorded using AJCC cri-
teria. Receiver operating characteristic analysis was used to discriminate the SLN size with the optimal sensitivity,
specificity and likelihood ratios (LR) for additional positive non-SLN. Results: Among 96 patients with a tumor posi-
tive SLN, 41% (n = 39) had micrometastasis, and 59% (n = 57) had macrometastasis. A positive non-SLN was identi-
fied after ALND among 18% (n = 7 of 39) with micrometastasis compared with 39% (n = 22 of 57) with macrometasta-
sis (p = 0.04). The size of the SLN metastasis and presence of additional tumor positive non-SLNs corresponds to a
positive likelihood ratio of 1.1 for micrometastasis and 1.6 for macrometastasis (95%CI: 0.56 - 0.74). Conclusions:
Increased size of tumor in SLN is associated with greater likelihood of non-SLN positivity and should be considered for
more aggressive follow-up and therapy.
Keywords: Sentinel Node; Axillary Lymph Node Dissection (ALND)
1. Introduction
Sentinel lymph node (SLN) biopsy is the standard method
for assessment of nodal involvement in clinically nega-
tive early breast lesions whereby only SLNs containing
metastasis require subsequent axillary lymph node dis-
section (ALND) [1]. Identification of the SLN allows
greater scrutiny of lymphatic tissue most likely to contain
metastasis via serial sectioning and immunohistochemi-
cal (IHC) analysis, improving the identification of small
tumor foci [2]. Improved pathologic methodology has
resulted in a greater than seven fold increase in the diag-
nosis of sentinel node micrometastasis (SNMM) over the
last decade [3]. To prevent stage migration, the classifi-
cation of “isolated tumor cells” was introduced as sepa-
rate category distinct from micrometastasis [4]. Isolated
tumor cells (ITC) are classified as node negative for treat-
ment and prognostic purposes whereas SNMM are con-
sidered positive and may necessitate additional axillary
Official guidelines from the American Society of Cli-
nical Oncology (ASCO) released in 2005 advise all pa-
tients with SLN micrometastasis to undergo completion
ALND, however, data from the National Cancer Insti-
tute’s Surveillance Epidemiology and End Results data-
base suggest that fewer than 60% of patients with
SNMM undergo additional axillary nodal clearance [1,3].
This change in clinicians’ attitude towards small volume
SLN metastasis is reflected in a 2009 ASCO survey
where 98.5% of those surveyed regard SNMM as impor-
tant—however only 23% of surgeons, 23% of medical
oncologists and 15% of radiation oncologists recommend
ALND for micrometastasis [5]. Although the prognostic
value of SNMM remains unclear, the extent of axillary
lymph involvement remains important for staging and
postoperative management. Since the introduction of
SLN biopsy, a proliferation of retrospective studies and
predictive models have emerged attempting to predict
the occurrence of additional non-sentinel lymph nodes
(non-SLN) containing tumor. The extent of SLN tumor
metastasis was previously associated with further axillary
*Corresponding author.
Copyright © 2012 SciRes. JCT
The Size of Metastasis in the Sentinel Node Is a Predictor of Additional Non-Sentinel Node Positivity 713
nodal positivity; the majority of studies are pooled co-
horts of early and advanced lesions combined in a single
analysis. Patients with small tumors and limited nodal
involvement may be ideal candidates for more limited
axillary interventions. With this in mind, we hypothe-
sized that size of SLN metastasis among early pathologic
T1 (pT1) cases will accurately predict additional non-
SLN positivity and may be useful in differentiating
which subgroups would benefit from more aggressive
axillary clearance strategies.
2. Materials and Methods
Patients and Tumor Characteristics. After approval of
the institutional review board for human research sub-
jects, a retrospective review of a prospectively collected
database identified patients who underwent sentinel node
biopsy for pT1 invasive breast cancer at Loyola Univer-
sity Medical Center between June 1999 and February
2010. Patients with primary tumors larger than 2 cm or
with pathology limited to ductal carcinoma in-situ were
Electronic medical records were reviewed for the fol-
lowing patient characteristics: age, sex, extent of breast
excision, size of primary tumor, Nottingham tumor grade,
tumor sub-classification, estrogen and progesterone re-
ceptor status, number of sentinel nodes (SN) removed,
frequency of SN containing tumor, size of SN metastasis,
presence of SN extranodal tumor extension, number of
non-SLNs removed, frequency of non-SLNs containing
tumor and peritumoral lymphovascular invasion.
Evaluation of Lymph Nodes. Sentinel nodes were
identified by preoperative injection of 99mTechnetium
labeled sulfur colloid and intradermal subareolar injec-
tion of vital blue dye (isosulfan or methylene blue). Sen-
tinel nodes were intraoperatively identified by visual blue
staining and using a hand held gamma counter. Subclas-
sification of SN size was according to AJCC Cancer
Staging Manual 7th ed.: small cell clusters of tumors up
to 0.2 mm or nonconfluent cells containing less than 200
cells per section were classified as isolated tumor cells
(ITC), metastasis greater than 0.2 mm and less than or
equal to 2.0 mm as micrometastasis, and nodal involve-
ment greater than 2.0 mm as macrometastasis [6,7]. Sen-
tinel nodes identified as ITC or micrometastasis were
independently confirmed by a single breast-trained pa-
thologist (P.R.).
The protocol for sectioning and evaluation of sentinel
nodes has been previously described. In brief, a 4 μm
section from sentinel node is taken for frozen section and
for permanent section the SN specimen is fixed in 10%
formalin, embedded in paraffin and stained with conven-
tional and eosin stain (H & E). Permanent sections that
do not show metastasis with H & E are serially sectioned
for three additional H&E staining and one immunohisto-
chemical (IHC) staining using a pankeratin antibody. Up
to four H & E sections and one IHC section are evaluated
before reporting a SLN as negative; any foci of metasta-
sis is measured and classified according to AJCC guide-
lines. When multiple foci of tumor are present the largest
width is used for staging purposes. Tumor histologic grade
was assessed using the Nottingham grading system [8].
Statistical Analysis. Continuous variables were de-
scribed as medians and interquartile ranges (25th - 75th
percentile). Normal distribution was assessed with the
D’Agostino-Pearson omnibus K2 test; because not all
data sets passed the normality test (α = 0.05), the
Mann-Whitney U test was used for continuous variables.
Fischer’s exact test and Pearson’s chi-square test were
used for dichotomous categorical variables. A two-tailed
p < 0.05 was considered significant. Receiver operating
characteristic (ROC) curves were created to determine
the SLN size with the optimal sensitivity and specificity
for additional non-SLN positivity. Sensitivity and speci-
ficity were used to calculate the positive likelihood ratio
(+LR) for additional non-SLN positivity (+LR = sensi-
tivity/1-specificity = true positives/false positives). The
+LR estimates how a positive test result (SLN exceeds a
particular threshold) changes the odds of having addi-
tional positive non-SLNs. The higher the +LR, the higher
the increase in odds of disease given a positive test. Sta-
tistical analyses were calculated with Stata/IC 11.0 for
Mac OS X (StataCorp) and GraphPad Prism 5 for Mac
OS X (GraphPad Software Inc.).
3. Results
A total of 483 patients with pT1 invasive breast cancer
underwent sentinel node biopsy and resection of the as-
sociated primary malignancy with either breast conserv-
ing surgery or mastectomy. Of this group, a positive SLN
was identified in 96 cases (19.9%), consisting of 40.6%
(39/96) micrometastasis and 59.4% (57/96) macrometas-
tasis. An additional 8 cases of ITC (7.7%) were observed;
these SLN were not classified as a positive SLN biopsy
and were included only in the ROC curve analysis as the
lowest cut point. Patient demographics and lymph node
features are shown in Table 1. Significant differences
were noted in method of pathologic detection among
groups. The majority of macrometastasis were seen on H
& E whereas micrometastasis were predominantly iden-
tified using immunohistochemistry. Sentinel node mac-
rometastasis were significantly more likely to demon-
strate extranodal tumor extension. As illustrated in Fig-
ure 1, sentinel nodes containing macrometastasis had a
greater frequency of tumor positive non-SLN (38.6%
22/57) when compared to SLN containing micrometasta-
sis (17.9%, 7/39, p = 0.04). The number of total positive
non-SLN in each instance was significantly greater for
SLN containing macrometastasis (Table 1, p = 0.02).
Copyright © 2012 SciRes. JCT
The Size of Metastasis in the Sentinel Node Is a Predictor of Additional Non-Sentinel Node Positivity
Table 1. Patient data and lymph node features among pa-
tients with positive sentinel lymph nodes.
Micrometastasis Macrometastasisp value
N = 39 (%) N = 57 (%)
Median age, yrs (IQR) 58 (47 - 71) 56 (47 - 67) 0.71
Age < 50 years 14 (35.9) 17 (29.8) 0.27
Age > 70 years 9 (23.1) 11 (19.3%) 0.80
Partial mastectomy 28 (71.8) 39 (68.4) 0.82
Mastectomy 11 (28.2) 18 (31.6) 0.72
Sentinel lymph nodes
Median no. SLN
removed, (IQR) 2 (1 - 3) 2 (1 - 3) 0.25
Median size SLN
metastasis, cm (IQR) 0.14 (0.1 - 0.2) 0.7 (0.25 - 1.1)<0.0001*
Detection by H & E
stain 24 (61.5) 52 (91.2) 0.0007*
Detection by pankeratin
IHC 23 (59.0) 7 (12.3) <0.0001*
Extrahilar nodal
extenstion 1 (2.6) 23 (40.4) <0.0001*
Axillary lymph node
Median no. non-SLN
removed, (IQR) 11 (2 - 17) 14 (10 - 18) 0.06
Median no. non-SLN
with tumor, (IQR) 1 (1 - 3) 2 (1 - 5) 0.02*
Freq. non-SLN positve
on ALND 7 (17.9) 22 (38.6) 0.04*
*statistically significant p < 0.05; IQR: Interquartile Range (25th - 75th
percentile); SLN: Sentinel Lymph Nodes; H & E: Hematoxylin & Eosin;
IHC: Immunohistochemistry; ALND: Axillary Lymph Node Dissection.
Figure 1. Frequenc y of non-sentinel lymph nodes (non-SLN)
containing metastasis stratified according to the size of tu-
mor in the sentinel node biopsy. Additional positive non-
SLNs identified in SLN with micrometastasis 17.9% (7/39)
versus 38.6% (22/57) in SLN containing macrometastasis
(*p = 0.04).
Features of the primary tumors in both subsets were
also compared as shown in Table 2. Among the 96 pa-
tients with a positive SLN biopsy there was no difference
in breast pathology between groups. The median size of
the primary tumor was significantly larger among cases
of macrometastasis. No significant differences were ob-
served between classifications of SLN metastasis for
Nottingham grade, estrogen and progesterone receptor
status, as well as peritumoral lymphovascular invasion.
The results of Table 3 and Figure 2 summarize the
association between increasing SLN tumor size and the
likelihood of an additional positive non-SLN. The posi-
tive likelihood ratio for additional non-SLN metastasis is
approximately 1.1 for micrometastasis and 1.6 in the case
of micrometastasis (95% CI 0.55 - 0.74). The ROC curve
shows that increasing the size of SLN metastasis im-
proves the specificity for identifying positive non-SLN
while maintaining sensitivity corresponding to an area
under the curve (AUC) of 0.6502.
4. Discussion
In the present study we demonstrate an association be-
tween the size of metastasis in the SLN and the presence
of additional positive non-SLN in pT1 invasive breast
cancer. Both SLN micro and macrometastasis have an
increased likelihood of additional positive non-SLNs.
Table 2. Features of primary tumors with sentinel nodes
containing metastasis.
Micrometastasis Macrometastasisp value
N = 39 (%) N = 57 (%)
Primary tumor
Median size, cm (IQR) 1.2 (0.7 - 1.5) 1.4 (0.1 - 2.0) 0.01*
Median Nottingham
grade, (gr. 1,2,3) 2 (1 - 2) 2 (1 - 2) 0.51
Infiltrating ductal 29 (74.4) 40 (70.2) 0.82
Infiltrating lobular 6 (15.4) 9 (15.8) 0.95
Other 4 (10.3) 8 (14.0) 0.58
Receptor status
ER+/PR+ 30 (76.9) 42 (73.7) 0.81
ER+/PR- 1 (2.6) 7 (12.3) 0.14
ER/PR+ 3 (7.7) 2 (3.5) 0.39
ER/PR 5 (12.8) 6 (10.5) 0.75
invasion, no. (%) 10 (25.6) 17 (29.8) 0.82
*statistically significant p < 0.05; IQR: Interquartile Range (25th - 75th
percentile); gr: Grade; ER: Estrogen Receptor; PR: Progesterone Receptor.
Copyright © 2012 SciRes. JCT
The Size of Metastasis in the Sentinel Node Is a Predictor of Additional Non-Sentinel Node Positivity 715
Table 3. Receiver operating characteristic analysis of non-
sentinel lymph nodes.
Status of Non-SLN
Size SLN
Metastasis Negative Positive Sensitivity Specificity+ L.R.
Isolated Tumor
Cells 8 0 100% 0% 1.00
Micrometastasis 7 32 100% 10.0% 1.13
Macrometastasis 22 35 75.9% 51.4% 1.56
ROC Area 0.6502
Standard Error 0.048
95% CI 0.56 - 0.74*
*statistically significant; ROC: Receiver operating characteristic; Non-SLN:
Non-Sentinel Lymph Nodes.
Figure 2. Nonparametric receiver operating characteristic
curve identifies the threshold of a positive screening test
that optimizes sensitivity and specific ity as expressed by the
area under curve (AUC). Increasing the size of SLN metas-
tasis improves the specificity for identifying positive non-
SLN with an AUC = 0.6502 (S.E. 0.048. 95% CI 0.56 - 074).
Increasing the size of tumor in SLNs corresponds to a
greater than two fold increase in the prevalence of
non-SLN metastasis, from 17.9% among micrometastasis
to 38.6% with macrometastasis. A positive SLN biopsy
will increase the odds of additional non-SLN metastasis
by a factor of 1.1 in micrometastasis and by nearly 1.6
when macrometastasis is present.
The size of the primary tumor within the pT1 subclass
was also associated with non-SLNs containing metastasis.
Extranodal tumor extension found predominantly in SLN
macrometastasis was also associated with positive non-
SLNs on univariate analysis. The association between
extranodal tumor extension, macrometastasis and axillary
nodal dissemination is demonstrative of the increased
metastatic potential of larger neoplasms. Previous studies
have shown more aggressive patterns of tumor spread
when peritumoral lymphovascular invasion is present
[9,10]. The present study did not find differences in the
occurrence of peritumoral lymphovascular invasion nor a
tendency for nodal spread among cases of SLN micro
and macrometastasis.
Both the size of the primary lesion and the extent of
regional metastasis are mutually reflective of the tumor’s
growth potential. Turner, et al identified a similar in-
crease in non-SLN positivity among pT1-T4 lesions with
larger primary tumors and increasing SLN tumor burden.
In this study, SLN micrometastasis corresponded to a
26% incidence of non-sentinel nodal positivity and a
63% occurrence for SLN containing macrometastasis [9].
In other case series limited to pT1-T2 neoplasms, the
frequency of non-SLN positivity ranges from 6% - 22%
for SLN with micrometastasis and 44% - 55% for mac-
rometastasis [10-12]. In a meta-analysis of 25 articles
reporting non-SLN spread concurrent with small volume
SLN metastasis, Cserni, et al report a risk of additional
axillary disease ranging from 10% - 15% [13]. The trend
towards decreased incidence of non-SLN metastasis cor-
responding to smaller primary tumors was also reflected
in the present study.
There are several explanations for the variability that
is noted among retrospective reviews attempting to quan-
tify and correlate sizing of SLN metastasis. Studies were
routine ALND was performed regardless of SLN status
may have higher estimates of non-SLN positivity com-
pared to those study protocols allowing omission of sur-
gical axillary clearance. [13] side from selection biases,
the method of pathologic detection will affect the sensi-
tivity-specifically the utilization of H & E versus IHC.
As noted in the present study, H & E was more often util-
ized for identifying macrometastasis whereas pankeratin
IHC was more frequently utilized for micrometastasis.
Although the association between small volume SLN
metastasis and additional non-SLN is clearly applicable
to early pT1 tumors, the clinical significance is less cer-
tain. Official guidelines from an ASCO panel of experts
continue to recommend ALND in the presence of micro
and macrometastasis on SLN biopsy. This has been
called into question by the recent publication from the
ACOSOG Z0011 trial showing no difference in local or
regional recurrence among patients with limited disease
randomized to SLND alone versus SLND followed by
ALND [14]. Participants of this study received lumpec-
tomy and opposing tangential whole field radiation for
T1 or T2 N0 M0 disease. Standard opposing tangential
field radiation is known to concurrently irradiate portions
of the level I and II axillary lymph nodes and may have
an effect on axillary recurrence notwithstanding the dif-
ferences in surgical axillary clearance [15,16]. The num-
ber of positive axillary lymph nodes remains a relevant
risk factor for local recurrence among patients undergo-
ing mastectomy without radiotherapy [17]. The effect of
ACOSOG Z0011 trial is further confounded by the ad-
Copyright © 2012 SciRes. JCT
The Size of Metastasis in the Sentinel Node Is a Predictor of Additional Non-Sentinel Node Positivity
ministration of adjuvant systemic therapy known to re-
duce locoregional recurrence. Patients who do not re-
ceive radiation and adjuvant systemic therapy may not
achieve the same results as in the Z0011 trial and may
still benefit from additional scrutiny of their axillary
nodal status.
5. Conclusion
The present study demonstrates a significant correlation
between the size of tumor in the SLN and axillary me-
tastasis to non-SLN in patients with pT1 breast cancer.
The size of the SLN metastasis is an important risk factor
even among early breast lesions. Although the strength of
association is strongest for patients with macrometastasis,
our data suggests that patients with either micro or mac-
rometastasis in their SLN biopsies have an increased
likelihood of additional nodal positivity. This has impor-
tant therapeutic implications given the recent trend to-
wards minimizing axillary interventions in perceived low
risk subpopulations. The findings of this study suggest
patients with pT1 lesions and large volumes of SLN tu-
mor should be considered for closer follow-up and more
aggressive axillary management strategies.
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