Journal of Cancer Therapy, 2013, 4, 1-6
http://dx.doi.org/10.4236/jct.2013.47A001 Published Online August 2013 (http://www.scirp.org/journal/jct) 1
A Comparison of Breast Surgeon and
Nomogram-Generated Risk Predictions of
Sentinel and Non-Sentinel Node Metastases*
Luisa Sugaya1, Paulo R. de Alcantara Filho1,2, Bruna Salani Mota1, Sujata Patil3,
Kimberly J. Van Zee2, José Luiz B. Bevilacqua1#
1Hospital Sirio-Libanes, Sao Paulo, Brazil; 2Breast Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, New
York, USA; 3Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, USA.
Received June 3rd, 2013; revised July 2nd, 2013; accepted July 9th, 2013
Copyright © 2013 Luisa Sugaya et al. This is an open access article distributed under the Creative Commons Attribution Li-
cense, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly
cited.
ABSTRACT
Memorial Sloan-Kettering Cancer Center (MSKCC) has developed 2 nomograms: the Sentinel Lymph Node Nomo-
gram (SLNN), which is used to predict the lik elihood of sentin el lymph node (SLN ) metastases in patien ts with invasive
breast cancer, and the Non-Sentinel Lymph Node Nomogram (NSLNN), which is used to predict the likelihood of re-
sidual axillary disease after a positive SLN biopsy. Our purpose was to compare the accuracy of MSKCC nomogram
predictions with those made by breast surgeons. Two questionnaires were built with characteristics of two sets of 33
randomly selected patients from the MSKCC Sentinel Node Database. The first included only patients with invasive
breast cancer, and the second included only patients with invasive breast cancer and positive SLN biopsy. 26 randomly
selected Brazilian breast surgeons were asked abou t the probability of each patient in the first set having SLN metasta-
ses and each patient in the second set having additional non-SLN metastases. The predictions of the nomograms and
breast surgeons were compared. There was no correlation between nomogram risk predictions and breast surgeon risk
prediction estimates for either the SLNN or the NSLNN. The area under the receiver operating characteristics curves
(AUCs) were 0.871 and 0.657 for SLNN and breast surgeons, respectively (p < 0.0001), and 0.889 and 0.575 for the
NSLNN and breast surgeons, respectively (p < 0.0001). The nomograms were significantly more accurate as prediction
tools than the risk predictions of breast surgeons in Brazil. This study demonstrates the potential utility of both nomo-
grams in the decision-making process for patients with invasive breast cancer.
Keywords: Sentinel Lymph Node Biopsy; Nomogram; Predictions; Breast Cancer; Completion Axillary Lymph Node
Dissection
1. Introduction
Over the last decades, public awareness, medical edu-
cation, and increased use of screening mammography
have resulted in earlier detection and treatment of invasive
breast cancer, greatly improving the prognosis of those
patients [1 ,2]. The adopti on of sentinel ly mph node bi opsy
(SLNB) has allowed those with no ax illary metastases to
avoid axillary lymph node dissection (ALND), and has
reduced morbidity as a result. Since the adoption of SLNB
to stage the axilla, the stand ard management of a positive
SLNB has included ALND. However, only 40% - 50% of
patients with positive sentinel lymph nodes (SLNs) who
undergo completion axillary lymph node dissection (cALND)
have additional non-SLN metastases, with favorable sub-
sets of women having an even lower risk of non-SLN
metastases. Women without residual nodal disease are
unlikely to benefit from cALND, but are exposed to the
risk of lymphedema and other morbidities.
A recent randomized co ntrolled tr ial of cALND (Ame-
rican College of Surgeons Oncology Group [ACOSOG]
Z0011) was carried out in a selected group of clinically
node-negative women with early-stage breast cancer un-
dergoing breast-conserving surgery and whole breast
radiation, with positive SLN. With over 6 years of follow-
*The authors have no conflicts of intere st to declare. The autho rs have
no funding sources to declare.
#Corresponding author.

A Comparison of Breast Surgeon and Nomogram-Generated Risk Predictions of Sentinel and Non-Sentinel
Node Metastases
2
up, no statistically significant differences in local or re-
gional recurrence were found in the groups that had SLNB
alone and those that underwent cALND [3]. These find-
ings support previous studies that suggested there is a
subgroup of patients with favorable characteristics who
could avoid ALND and be treated with breast-conserving
surgery, radiotherapy, and adjuvant systemic therapy [4-
9].
A recent study from Memorial Sloan-Kettering Cancer
Center (MSKCC) analyzed the possible impact of Z0011
on the rate of ALND using the criteria of that trial [10].
The study concluded that if the Z0011 trial criteria were
applied to the MSKCC SLN database popul ation, the need
for ALN D would ha ve been reduc ed by 13% i n the overall
breast cancer patient population and by 48% in the subset
of patients with positive SLNs. In fact, in the United
States, many of those with SL N mi crometastases have not
been undergoing cALND; an analysis of the National
Cancer Data Base showed that in 2005 almost 50% of
those with microscopic metastases in the SLN did not
undergo ALND [11] .
In order to estimate the likelihood of SLN metastases or
to select women in whom the risk of having residual
axillary disease is low, it is necessary to weigh multiple,
different factors which have been shown to be predictive:
tumor; sentinel node; and patient characteristics. It is
difficult for a clinician to appropriately weigh all of the
various factors, which increase or decrease the risk of
disease simultaneously. Nomograms are useful tools that
improve the accuracy of clinical judgment [12-16] and
help clinicians to deal with these very complex tasks. No-
mograms are prediction instruments based on regression
analysis of multiple variables that translate complex cal-
culations to simple graphical tools or simple software. In
addition, nomograms also permit clinicians to provide
more precise and comprehensible in formation to p atients,
who are increasingly interested in their disease and who
are increasingly taking part in the decisions regarding
their treatment [17].
MSKCC has built 2 prognostic nomograms, one to
predict the lik elihood of SLN metastases in patients with
invasive brea st cancer (the MSKCC SLN nomogram ) [18],
and one to predict the likelihood of non-SLN metastases
in patients with a positive SLN biopsy (the MSKCC
Non-SLN nomogram) [19]. Both are available from the
MKSCC website at http://www.mskcc.org/cancer-care/
adult/breast/prediction-tools and at www.nomograms.org.
The MSKCC SLN nomogram (SLNN) incorporates 9 cha-
racteristics of primary breast cancer, includi ng age, tum or
size, tumor type, lymphovascular invasion, tumor location,
multifocality, nuclear grade, and presence of hormone
receptors. The MSKCC non-SLN nomogram (NSLNN)
includes the same variables, except for age and tumor
location, plus characteristics of the SLNs.
The NSLNN has been validated worldwide, showing its
robustness in populations different from the one in which
it was developed [20-24]. However, a no mogram’s utility
is determined by its superiority over clinical judgment
[25]. In contrast to use in the United States and Europe,
the use of nomograms in Brazil and other developing
countries is limited. Here we seek to compare the risk
predictions of SLN metastases generated by both nomo-
grams with risk predictions of SLN metastases based on
the clinical judgment of breast surgeons in Brazil.
2. Materials and Methods
This project was approved by the Institutional Review
Boards of Hospital SírioLibanês, São Paulo, Brazil
(HSL2008/13) and MSKCC. The NSLNN and SLNN
were each developed in a training population, and each
was then tested in an independent validation population
from MSKCC [18,19]. For the present study, all patient
data were de-identified. We randomly selected 33 cases
from each of the validation populations used to test the
original no mograms.
Of 166 breast surgeons registered with the Brazilian
Society of Breast Surgeons and work ing in São Paulo, we
randomly selected 81 participants. Twenty-six breast
surgeons agreed to participate; the others either declined
to participate (n = 7) or were unable to be contacted (n =
48). All participants were volunteers and provided signed
informed consent. Most of these breast surgeons were
unfamiliar with the nomograms, and none had incorpo-
rated their use into their clinical practice at the time of the
study.
Two questionnaires were adm inistered to each surgeon.
In the first, data from 33 patients randomly selected from
the SLNN validation population were provided: age; tu-
mor size; tumor type; presence of lymphovascular inva-
sion; tumor location; multifocality; nuclear grade; and
estrogen and progesterone receptor status. For each pa-
tient, breast surgeons were asked: “Of 100 women with
invasive breast cancer with these characteristics, how
many of them would you expect to have one or more po-
sitive sentinel lymph nodes?”
In the second questionnaire, data were presented from
33 cases from the NSLNN validation population: patho-
logical size; tumor type; nuclear grade; lymphovascular
invasion; multifocality and estrogen-receptor status of the
primary tumor; method of detection of SLN metastases;
number of positive SLNs; and number of negative SLNs.
Breast surgeons were asked: “If 100 women with a positive
sentinel node had these characteristics and then received a
full axillary dissection, how many of them wou ld yo u e x-
pect to have one or more positive non-sentinel lymph
nodes?”
When a response was provided as a range, the highest

A Comparison of Breast Surgeon and Nomogram-Generated Risk Predictions of Sentinel and Non-Sentinel
Node Metastases 3
value was used. Breast surgeon risk predictions were
plotted against MSKCC nomogram risk predictions to
assess correlation. To compare the accuracy of each no-
mogram’s risk predictions with those of the breast sur-
geons, we calculated the area under the recei ver operating
curve (AUC-ROC). AUC estimates and standard errors
were calculated using bootstrap methods to account for
each patient having been evaluated once by each sur-
geon.
To compare the AUCs for each nomogram and from the
surgeon estimates, we used bootstrap methods. Specifi-
cally, we bootstrapped each of the 33 scenarios 200 times
and calculated the AUCs for the nomogram risk predic-
tions and surgeon risk predictions for each bootstrapped
dataset. The differences were tested using a paired t-test.
3. Results
Twenty-six breast surgeons, 32.1% of our initial sample,
answered the 2 questionnaires completely. Histograms of
the nomogram predictions and surgeon estimates by ac-
tual outcomes revealed different distributions for the no-
mograms and breast surgeons (Figures 1 and 2). In both
scenarios, the nomogram predictions better differentiated
negative and positive outcomes, particularly when pre-
dicting the presence of residual axillary diseases after a
positive SLN biopsy (Figure 2). The predictions of breast
surgeons were similar for cases with positive and negative
outcomes.
When predicting the likelihood of a patient having SLN
metastases, the AUC-ROC achieved by the MSKCC
nomograms was 0.871 (Figure 3). In comparison, the
AUC-ROC achieved by the breast surgeons in our study
was 0.657 (p < 0.0001) (Figure 3). When predicting the
likelihood of a patient having non-SLN metastases when
Figure 1. Distribution of sentinel lymph node nomogram
(SLNN) and breast surgeon predictions of risk of SLN me-
tastasis, by actual outcome.
Figure 2. Distribution of non-sentinel lymph node no-
mogram (NSLNN) and breast surgeon predictions of risk of
additional nodal metastases in a woman with a positive sen-
tinel node, by actual outcome.
Figure 3. Receiver operating curves for: (A) SLN-nomo-
gram and SLN breast surgeon risk predicitions; and (B)
non-SLN nomogram and non-SLN breast surgeon risk pre-
dictions.
their SLN was positive, the AUC-ROC achieved by the
nomogra m was 0. 889 (Figure 3); whereas the AUC-ROC
achieved by clinical experts was 0.575 (p < 0.0001) (Fig-
ure 3).
4. Discussion
To our knowledge, this is the first study to compare risk
predictions of SLN m etastases m ade by clini cal experts to

A Comparison of Breast Surgeon and Nomogram-Generated Risk Predictions of Sentinel and Non-Sentinel
Node Metastases
4
those gener ated by MSKC C’s 2 nom ograms. Our findin gs
are in agreement with previous studies [15,25,26] sug-
gesting that nomograms outperform clinicians in pre-
dicting clinical outcomes related to multiple variables.
And, similar to prior studies [25,26], we found that the
NSLNN was more accurate than the breast surgeons in
our study in predicting the likelihood of non-SLN me-
tastases in patients with positive SLN biopsy. Our find-
ings suppor t the utility of nomograms in p redicting these
outcomes.
Several factors may explain the superior accuracy of
the MSKCC nomograms. The use of regression models
ensures that each variable contributes to the results based
on their actual predictive power and relation to the crite-
rion of interest. Therefore, if using the same data, nomo-
grams always lead to the same conclusion, preventing the
influence of random factors that often bias clinical
judgment [27]. Furthermore, for clinicians, it is difficult
to clearly distinguish between valid and invalid variables,
and false beliefs often develop regarding associations
between variables. Recall bias, control bias, fatigue, and
clinical experience can also influence clinical judgment
[28]. Nomograms translate complex equations through
simple graphics or software, and are powerful tools that
help clinicians and patients balance benefits and risks,
while managing the diagnosis and treatment of the dis-
ease.
The recently published ACOSOG Z0011 randomized
controlled trial of axillary node dissection in a selected
group of women with early-stage breast cancer and posi-
tive SLN underg oin g whole b reast radiation and systemic
adjuvant treatment suggested that in women with a low
risk of furt her met astasis, ALND m ay have no therapeut ic
benefit [3] and results in increased morbidity [29-34].
During the last decade, after the introduction of the
NSLNN, there has been a declining rate of ALND in
patients with positive SLN [11,19], and several groups
have reported a very low rate (<1%) of axillary recurrence
among patients selected to no t undergo ALND [6,35- 37].
At MSKCC, when compared to those patients who did
undergo cALND after a positive SLN, patients who did
not undergo A LND were older, more likely to have breast
conservation, and had smaller tumors, fewer high-grade
lesions, less lymphovascular invasion, and lower nomo-
gram scores o verall [8], suggest ing that the nomogram did
identify a group at low risk of axillary recurrence.
The universal use of SLN biopsy is less controversial
than that of cALND, and therefore, the SLNN would not
often result in a change in surgical decision making.
However, the SLNN nomogram helps a breast surgeon
explain to a woman the risk of nodal metastasis of her
disease. The absolute risk prediction provided by the no-
mogram is much more useful than knowing a list of risk
factors, each associated with a hazard ratio, a nd can as sist
in patient education and decision making.
Nevertheless , i t is cle ar that n omo grams cannot repl ace
clinical judgment. In deciding whether or not to perform
SLN biopsy or completion ALND, breast surgeons also
need to consider inaccuracies in the diagnoses, uncer-
tainties about the progression of the disease, variable
responses to treatme nt, im plica tions for system ic therapy,
and the individual characteristics of each patient, such as
age and psychological factors [38].
With the result s of ACOSOG Z0011, t he increasing use
of nomograms, the development of more accurate tools
[39,40], and a clearer identification of a subgroup of pa-
tients who can safely avoid such procedures, breast sur-
geons in Brazil may be encouraged to include the nomo-
grams in their decision-m aking proc esses after disc ussing
both related advantages and disadvantages, and the im-
pact of avoiding the completion of ALND.
One may argue that the major limitation of the recent
randomized Z0011 trial is that of low external validity
because that trial selected patients at very low risk of
additional metastases. Indeed, the authors of that trial
state that “most of the patients in this trial had a low
axillary tumor burden” [3]. Caution at the initiation of the
study led to an attempt to assure that women with high
tumor burden were not randomized to SLND alone. The
Z0011 trial exc luded patients wh o underwent m astectomy,
had clinically palpable lymph nodes, had 3 or more posi-
tive SLNs, had large tumors, and who received neoadju-
vant treatment. As a result of these careful selection cri-
teria, in the women randomized to ALND, only 27% had
additional nodal disease identified. This is significantly
lower than the more typical rate of 40% - 50% in most
unselected series of clinically node-negative wo men who
are found to have a positive SLN [19,39]. According to
NCCN guidelines [41], completion ALND is still a
standard of care for positive-SLN patients, especially in
those patients who d o not fulfill the criteria of ACOSOG
Z0011 (women with larger tumors; women with clinically
palpable nodes or 3 or more positive SLNs; women un-
dergoing mastectomy or lumpectomy without whole
breast radiation). For this population, the nomogram is a
useful tool to predict ad ditional metastasis.
Although all the d ata in this study that were presented
to the breast surgeons were taken from real cases, clinical
decisions based on hypothetical situations may not re-
produce real clinical scenarios. Other variables, such as
years of practice, the type of hospital that the breast sur-
geon interviewed worked at, previous contact with other
nomograms, and willingness to participate in the study
may also have influenced the results. The AUC-ROC of
both nomograms were larger than the ones found in the
original studies [18,19], and we randomly selected the

A Comparison of Breast Surgeon and Nomogram-Generated Risk Predictions of Sentinel and Non-Sentinel
Node Metastases 5
cases for our questionnaires from patients that were not
included in the nomogram development populations.
In order to achieve more individualized treatment of
patients with breast cancer, breast surgeons will need to
accurately predict the probability of a patient having
additional disease. Our study demonstrates that the risk
predictions of both nomograms were more precise than
the risk predictions estimated by breast surgeons, dem-
onstrating the potential utility of both nomograms in the
decision-making process for patients with invasive breast
cancer.
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