Journal of Cancer Therapy, 2012, 3, 846-852 Published Online October 2012 (
Axillary Recurrences after Sentinel Node Surgery—Results
over Ten Years in a University Hospital
Helle Eilertsen1, Ellen Schlichting2, Marianne Efskind Harr3, Daehoon Park4, Torill Sauer1,5,
Siri Larønningen6, Rolf Kaaresen1,2*
1Medical Faculty, University of Oslo, Oslo, Norway; 2Department of Breast and Endocrine Surgery, Oslo University Hospital, Oslo,
Norway; 3Department of Neurosurgery, Oslo University Hospital, Oslo, Norway; 4Department of Pathology, Vestre Viken Hospital,
Drammen, Norway; 5Department of Pathology, Oslo University Hospital, Oslo, Norway; 6Cancer Registry of Norway, Oslo, Norway.
Email: *
Received July 10th, 2012; revised August 15th, 2012; accepted August 27th, 2012
Background: Sentinel node biopsy (SNB) was introduced at Ullevaal University Hospital in 2000. This article presents
results from the first ten years use of the method. Material and Methods: A prospective registration of 2762 patients
was made from 2000 through 2009. Results: The median follow-up time was 51 months. The overall detection rate was
93%. 36% of the patients with positive SNs had non-sentinel metastases. These were significantly associated with a
macrometastatic SN and a primary tumour > 20 mm. 18% of patients with sentinel metastasis 2 mm had non-sentinel
metastases. 14 patients with negative SN (0.7%) developed axillary recurrence. 32% with a preoperative diagnosis of
ductal carcinoma in situ (DCIS) were upstaged to infiltrating carcinoma on final histology. None of the patients with
pure DCIS had positive SNs. Conclusion: Few late events (0.7%) in SN negative axillas demonstrate the safety of the
Keywords: Breast Cancer; Ductal Carcinoma in Situ; Sentinel Node; Non-Sentinel Metastasis; Axillary Recurrence
1. Introduction
As one of the first hospitals in Norway, Ullevaal Univer-
sity Hospital introduced sentinel node biopsy (SNB) as a
routine method in March 2000.
Between 400 and 500 patients were diagnosed with
breast cancer in the hospital per year during the study
We present the results from the first ten years using the
SNB technique with a particular focus on three aspects:
- Axillary recurrences in patients with negative SN in
the first operation;
- The correlation between size of SN metastasis and the
risk of metastasizing to non-SN lymph nodes;
- The role of SN biopsy in patients with a preoperative
diagnosis of ductal carcinoma in situ (DCIS).
2. Patients and Methods
Between March 2000 and December 2009, 2762 patients
(2751 women and 11 men) with breast cancer underwent
SNB at Ullevaal University Hospital. 36 patients had
bilateral surgery and thus 2798 SNBs were performed
during the study period. The median age was 58 years
(22 - 92). 85% of the patients had preoperative diagnosis
of DCIS or infiltrating carcinoma by either fine needle
aspiration cytology (FNAC) or core biopsy, the rest by
surgical biopsy.
2.1. Registration of Data
A prospective, scheme based registration was used. The
data was kept in an internal hospital database with the
acceptance from the relevant authorities.
2.2. Inclusion and Exclusion Criteria
For the first 5 years patients 75 year with a preopera-
tively estimated tumour size 3 cm were included. The
last 5 years also patients with tumours between 3 and 5
cm were included with no upper age limit.
The exclusion criteria for the entire period were pa-
tients with cytologically verified axillary metastases and
those who had preoperative chemotherapy. During the
first 5 years DCIS and multifocal disease were exclusion
criteria, but for the last 5 years multifocality and DCIS
grade III on cytology or histology were included.
2.3. Identification of the Sentinel Node
Both blue dye and radioactivity were used to identify the
*Corresponding author.
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Axillary Recurrences after Sentinel Node SurgeryResults over Ten Years in a University Hospital 847
SN. For the first 6 years, blue dye (One ml patent blue
diluted to 5 ml with isotone saline) and radioactivity (80
mBq in 08 ml) were injected peritumourally. From Janu-
ary 2006 the injection was made periareolarly. Radioac-
tivity was injected the day before surgery, whereas blue
dye was injected after the patients were under general
A lymph node was defined as a SN if the radioactivity
was at least ten times the background activity, whereas
the degree of colour was determined by a subjective as-
sessment by the surgeon.
2.4. Histopathological Examination of Sentinel
All sentinel nodes were intraoperatively sent to frozen
section examination. The nodes were bisected along the
longitudinal axis and 2 - 3 frozen sections were cut from
each cut surface. About 8 - 12 sections were examined
per lymph node. All SNs were later formalin fixated,
paraffin embedded and stained with hematoxylin-eosin
and examined as part of the final histological evaluation.
(Figure 1) In cases of doubt, immunohistochemical test-
ing was performed [1].
2.5. Axillary Lymph Node Dissection
Axillary lymph node dissection (ALND) was performed
if the SN was positive either intraoperatively or after
final histological assessment. In the case of a negative
SN intraoperatively, the patient was reoperated if final
histology found a metastasis. Patients found to have SNs
with isolated tumour cells (metastasis < 0.2 mm) did not
undergo ALND, according to the guidelines of the Nor-
wegian Breast Cancer Group (NBCG) [2].
2.6. Reevaluation of Positive SNs
Positive SNs were later re-examined and the largest di-
ameter of metastasis remeasured by an independent pa-
Figure 1. Hematoxylin and eosin stained sentinel node with
metastasis from an infiltrating ductal carcinoma, micro
papilary subtype.
thologist (DP) blinded for other data.
2.7. Definition of Axillary Recurrence
Axillary recurrence was defined as detection of cancer
cells in the axilla more than 120 days after the date of
primary axillary surgery. The reports of axillary recur-
rences were found by searching the patient records in the
hospital verified and supplemented by the Cancer Regis-
try of Norway.
2.8. Statistical Analysis
Comparison of data between groups was made using chi-
square test and Fisher exact test. Multivariable analyses
were made using a multiple logistic regression model. A
two-tailed p-value of 0.05 or less was considered statis-
tically significant. Analyses were performed using SPSS
version 18.0 (SPSS Inc., Chicago, Illinois, USA).
3. Results
Median follow-up time was 51 months (0 - 117). Histo-
pathological tumour characteristics are given in Table 1.
3.1. Detection of Sentinel Node
The detection rate for the entire period was 93% (95% CI
92 - 94). Peritumoural injection of blue dye and radioac-
tivity gave a detection rate of 90% (95% CI 88 - 91),
whereas the detection rate with periareolar injection was
96% (95% CI 95 - 97). There was a significant difference
in detection rate after change of injection site (p < 0.001).
A total of 30 surgeons did the SN procedures. Their
detection rate did not differ significantly when grouped
according to the number of procedures they performed
(Table 2).
On multivariable analysis, neither age, tumour grade
or tumour size was found to be significant factors in the
detection of SN.
A median value of 1 node [1-8] was retrieved during
the SNB.
27% of the patients in whom SN was not found, had a
metastasis to one or more axillary nodes. The median
value of metastatic nodes after ALND was 3 (range 1 -
3.2. Positive Sentinel Nodes
A positive SN on final histopathological examination
was found in 620 (24%) of the 2586 patients where SN
was detected. The largest diameter of SN metastases in
each patient categorized in three groups is shown in Ta-
ble 3.
141 patients had an intraoperatively false negative SN
and were reoperated with ALND. The negative predict-
tive value of intraoperative SN assessment was 93%
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Axillary Recurrences after Sentinel Node SurgeryResults over Ten Years in a University Hospital
Table 1. Tumour characteristics of 2798 breast cancer pa-
tients. Missing data given in numbers only. The percentages
show the distribution of the parameter s in known cases.
Median invasive tumour size
(n = 2476, missing 41) 15 mm (range 0.5 - 86)
Histological type (n = 2776)
Ductal 1507 (54%)
Lobular 220 (8%)
DCIS 246 (9%)
Ductal + DCIS 623 (22%)
Other 180 (7%)
Missing 22
Histological grading of
invasive ductal carcinomas
(n = 1499)
1 469 (31%)
2 695 (47%)
3 335 (22%)
Missing 8
Oestrogen receptor status:
(n = 2456)
Positive 2059 (84%)
Negative 397 (16%)
Missing 61
Progesterone receptor status
(n = 2444)
Positive 1662 (68%)
Negative 782 (32%)
Missing 73
Her2 status (n = 1459*)
Positive 138 (9%)
Negative 1321 (91%)
Missing 39
*The registration of Her2 started in 2004.
Table 2. Detection rate related to total number of sentinel
node (SN) procedure s done by each surgeon.
Total SN
procedures per
30 >30 100 >100 400>400
Det. Rate
[95% CI]
[86 - 95]
[91 - 97]
[91 - 94]
[91 - 94]
(95% CI 92 - 94). Of the patients with an intraoperatively
false negative SN, 71% had micrometastasis 2 mm.
On multivariable analysis, tumour size > 20 mm had a
significant association to positive sentinel nodes (p <
0.001), whereas tumour grade and receptor status had no
significant correlation.
3.3. Non-SN Metastases in Patients with Positive
Of the patients with positive SN, 36% had metastasized
also to non-sentinel lymph nodes.
There was a significant difference in the share of
non-SN metastases in correlation with size of the SN
metastasis (p < 0.001) (Table 4).
A multivariable analysis comparing SN positive pa-
tients with and without non-sentinel metastasis, found
that the only other characteristic, apart from size of SN
metastasis, was size of primary tumour. A significant
difference was seen between patients with tumours
smaller than and larger than 20 mm (p = 0.013).
3.4. Positive Sentinel Node in Ductal Carcinoma
in Situ Grade III
There were 225 patients with DCIS grade III on either
FNAC or core biopsy. Of these, 72 (32%) had infiltrating
carcinoma on final histology. Of the 211 patients with a
preoperative DCIS grade III diagnosis that we have data
on, 23 had a positive SN (11%), 11 of which had micro-
metastasis 2 mm. None of the patients with DCIS on
final histology had a positive SN.
3.5. Axillary Recurrences in SN Negative
Of those with negative SN, axillary recurrence was seen
in 14 patients (0.7%). The median interval of months
between time of surgery and registered date of axillary
recurrence was 24 (range 4 - 34).
A comparison of tumour characteristics of patients
with and without axillary recurrences, showed significant
differences for grade 3 tumours (p = 0.012), but not for
age, size or receptor status (Table 5).
Ki67 expression was seen in 92% of the patients with
axillary recurrence.
Table 3. Largest diameter of sentinel node (SN) metastases.
Size 2 mm > 2 5 mm>5 mm
Share of SN metastases
(n = 620, 16 missing ) 170 (28%) 158 (26%) 276 (46%)
Table 4. Share of non-sentinel node (SN) metastasis related
to size of sentinel node metastasis.
Size (mm) 2 >2 5 >5
Non-SN metastasis
[95% CI] 17% [12 - 23] 33% [26 - 40] 49% [43 - 55]
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Axillary Recurrences after Sentinel Node SurgeryResults over Ten Years in a University Hospital 849
Table 5. Tumour characteristics in patients with and with-
out axillary recurrence.
Patients with
negative SN,
n = 1966
Patients with axil-
lary recurrence,
n = 14
Median age
(years) 59 14 NS*
Grade 3 217/995 (22%)7/14 (50%) 0.012
Oestrogen receptor
negative 281/1667 (17%)4/12 (33%) NS*
receptor negative 544/1661 (33%)6/12 (50%) NS*
Median invasive
tumour size (mm) 14 13 NS*
*NS: Non significant.
4. Discussion
Our rate of axillary recurrences supports the conclusion
from other studies: A negative SN is a reliable indicator
of axillary status and omitting axillary dissection after
negative sentinel node biopsy is safe [9-14].
4.1. Detection Rate
Our overall detection rate is slightly lower than what is
reported in other studies [3-6], but meets the require-
ments set by NBCG. The significant difference in detec-
tion rate after change of injection site support the change
in guidelines made by NBCG [2] from peritumoral to
periareolar injection as the preferred method. As we
found no significant differences in identification rate
between the experienced and inexperienced surgeons, a
hypothesis that the detection rate was so low because of a
large number of inexperienced surgeons at our teaching
hospital failed. Further, no clinical or tumour characteris-
tics were found to be significant in detecting SN. This
suggests that the method is less dependent of the surgeon
and the patient population and more dependent on quali-
ties within the method itself. An explanation for the rela-
tively low detection rate might be our stringent definition
for a SN to have at least ten times the background radio-
activity. Most publications on the method does not define
this level and might have included nodes we excluded
due to too low levels of activity.
4.2. Non-Sentinel Node Metastases
Macrometastasis to SN and size of primary tumour are
significant predictors for the involvement of non-SN
metastasis. Similar findings have been reported in other
studies [6-8,15,16].
18% of our patients with a SN metastasis 2 mm had
further nodal involvement. A metaanalysis of 25 studies
found an incidence of further nodal involvement in 20%
of patients with micrometastasis or isolated tumour cells
to SN [17]. The literature has for years been contradict-
tory about micrometastases` influence on recurrence and
survival [7,9,18]. Guiliano et al. recently concluded in
their randomized controlled trial that ALND might no
longer be justified for women with small breast carcino-
mas and a positive SN as long as a set of specified adju-
vant therapies are given [19]. The Norwegian Breast
Cancer Group have decided that patients with SN metas-
tasis 2 mm should avoid having ALND if breast pre-
serving therapy including radiotherapy to the breast and
lower axilla is carried out [2]. Similar to Hulvat et al.
[20], we did not find any correlation between receptor
positivity and/or histology grade with either SN or non-
SN metastasis.
4.3. Sentinel Node Metastasis in Ductal
Carcinoma in Situ
The value of doing SNB in DCIS has been disputed;
some authors are in favour [10,11,21,22], others against
[9-11,15-19,21-25]. Most, however, agree that it should
be done in patients who undergo mastectomy, because
this eradicates the possibility to later perform SNB if
preoperative diagnosis of DCIS is changed to infiltrating
carcinoma [26-28].
None of the preoperative DCIS patients in our material,
who on final histology was found to have true DCIS had
positive SNs, whereas 11% of the patients that were up-
staged to infiltrating carcinoma did. Based on these re-
sults we find that omitting SNB in patients with pure
DCIS on final histology could be justified, whereas pa-
tients that on final histology have an infiltrating compo-
nent should undergo SNB. The large share of patients in
our material (32%) who were upstaged from a preopera-
tive diagnosis of DCIS grade III by FNAC or core biopsy
to infiltrating carcinoma on final histology, shows that
invasive foci are often overseen in the preoperative
Some studies [10,29,30] have looked at risk factors
among preoperative DCIS patients that can predict pres-
ence of an invasive component and thus who could bene-
fit from having SNB performed as part of the initial op-
eration. These studies have contradicting results and a
definite conclusion is thus not possible.
4.4. Axillary Recurrences
An axillary recurrence rate of 0.7% with a median follow
up time of 51 months is acceptable and in accordance
with the results from other studies. A recent study with a
median follow-up time similar to ours, found a recur-
rence rate of 0.7% [31], another reports an axillary re-
currence rate of 0.6% after a median follow up time of 37
months [32]. A systematic review and meta-analysis of
Copyright © 2012 SciRes. JCT
Axillary Recurrences after Sentinel Node SurgeryResults over Ten Years in a University Hospital
48 studies found a recurrence rate for axillary metastasis
in clinically node negative women with a primary nega-
tive SN of 0.3% after a median follow up time of 34
months [33].
Our results indicate that longer follow-up time does
not increase the rate of recurrence much, in accordance
with other studies which observe that the majority of
recurrences happens during the first two years after di-
agnosis [5,19,34].
Apart from a significant higher share of grade 3 tu-
mours, we found no other significant characteristics in
the axillary recurrence population. Similar results were
reported by Kiluk et al. [35] and Bergquist et al. [32].
However, we had very few cases of recurrences in each
risk category, and the lack of significant relation of re-
currence to the other risk factors may be due to the low
number (n = 14) and thus lack of statistical power.
One explanation of the low axillary recurrence rate
might be that we have a low-risk population with a high
percentage of good prognostic factors such as small tu-
mour size (median 15 mm), oestrogen (84%) and pro-
gesterone (68%) positivity and a low frequency of poor
prognostic factors, such as lymph node involvement
(24%) and Her2 positivity (9%) (Table 1). This selection
is probably explained by the introduction of mammog-
raphy screening for women aged 50 - 69 in the hospital’s
referral area in 1996, four years prior to the introduction
of the SN procedure.
5. Conclusions
Few recurrences (0.7%) in SN negative axillas demon-
strate the safety of the technique. Apart from a signifi-
cant higher share of grade 3 tumours, we found no other
significant characteristics in the axillary recurrence popu-
lation. The median time to recurrence was 24 months.
The rather high frequency of patients with non-SN
metastases, also in those with micrometastasis (18%),
shows that removal of SN alone might not be sufficient
for local control of the axilla if axillary x-ray treatment is
not included.
The SN procedure seems unnecessary in patients with
histology proven DCIS not undergoing mastectomy.
6. Acknowledgements
Assistance with the finding and verification of recur-
rences by Ann Helen Seglem and Monica Johansen,
Cancer Registry of Norway is acknowledged.
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