Journal of Cancer Therapy, 2013, 4, 1395-1402
Published Online November 2013 (
Open Access JCT
Axillary Sentinel Lymph Node Biopsy for Breast Cancer
and Melanoma Patients after Previous Axillary Surgery:
A Systematic Review*
Maurice Matter1,2#, Sebastien Romy1,3, Ariane Boubaker4, Olivier Michielin2, Nicolas Demartines1
1Department of Visceral Surgery, Centre Hospitalier Universitaire Vaudois and University of Lausanne, Lausanne, Switzerland;
2Department of Oncology, Melanoma Outpatient Clinic, Centre Hospitalier Universitaire Vaudois and University of Lausanne,
Lausanne, Switzerland; 3Hôpital de Payerne, Payerne, Switzerland; 4Department of Nuclear Medicine, Centre Hospitalier Universi-
taire Vaudois and University of Lausanne, Lausa nne, Switzerland.
Received October 7th, 2013; revised October 30th, 2013; accepted November 7th, 2013
Copyright © 2013 Maurice Matter et al. This is an open access article distributed under the Creative Commons Attribution License,
which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Objective: Sentinel lymph node biopsy (SLNB) is a validated staging technique for breast carcinoma. Some women are
exposed to have a second SLNB due to breast cancer recurrence or a second neoplasia (breast or other). Due to modi-
fied anatomy, it has been claimed that previous axillary surgery represents a contra-indication to SLNB. Our objective
was to analyse the literature to assess if a second SLNB is to be recommended or not. Methods: For the present study,
we performed a review of all published data during the last 10 years on patients with previous axilla surgery and second
SLNB. Results: Our analysis shows that second SLNB is feasible in 70%. Extra-axillary SNs rate (31%) was higher
after radical lymph node dissection (ALND) (60% - 84%) than after SLNB alone (14% - 65%). Follow-up and com-
plementary ALND following negative and positiv e second SLNB shows that it is a reliab le procedu r e. Conclusion: The
review of literature confirms that SLNB is feasible after previous axillary dissectio n. Triple technique for SN mapping
is the best examination to highlight modified lymphatic anatomy and shows definitively where SLNB must be per-
formed. Surgery may be more demanding as patients may have more frequently extra-axillary SN only, like internal
mammary nodes. ALND can be avo ided when second SLNB harvests negative SNs. These conclusions should however
be taken with caution because of the heterogeneity of publications regarding SLNB and surgical technique.
Keywords: Breast Neoplasms; Melanoma; Sentinel Lymph Node Biopsy Dissection; Lymphatic Vessels; Surgery;
Lymphatic Anatomy
1. Background
Breast cancer has an incidence of 126/100,0 00 and is the
commonest neoplasm in women [1]. Risk for ipsilateral
breast cancer recurrence in women with early-stage
breast cancer and breast-conserving therapy is about 5%
- 20% [2]. On the other hand, melanoma has worldwide a
growing incidence [3]. It is the fourth commonest neo-
plasm in women with an incidence of about 15/100,000.
Distribution of melanoma location shows a high density
on the back, shoulders and upper arms in women [4]. It is
not definitively established if breast cancer incidence
after melanoma is increased or not compared to inci-
dence in the general population [5,6]. In a large registry
of 1926 men with breast cancer, Satram-Hoang showed
that relative risk for melanoma was 2.98 (relative risk of
52 for a second breast cancer) [7]. The study of Brower
et al. showed that breast cancer was the commonest non
skin second primary cancer in melanoma patients [8].
Due to these cancer incidences and some risks of re-
currence, it is likely that women could be exposed to two
sentinel lymph node biopsies (SLNB) or further surgery
following radical axillary lymph node dissection (ALND).
It has been initially claimed that previous axillary sur-
*Grant support: none.
Conflicts of interest statement: All authors disclose neither financial
nor personal relationships with other people or organisations that could
inappropriately influence their work.
#Corresponding author.
Axillary Sentinel Lymph Node Biopsy for Breast Cancer and Melanoma Patients after Previous Axillary Surgery:
A Systematic Review
gery would represent a contra-indication to SLNB in
breast cancer patients due to the modification of lym-
phatic anatomy [9]. Subsequent observations and case
studies have shown that 2 succeeding SLNB procedures
for recurrent ipsilateral breast cancer were feasible [10].
Our tertiary academic centre includes a melanoma
clinic run by medical and surgical oncologists and an
accredited breast cancer centre. After facing patients with
melanoma and a past medical history of SLNB for breast
cancer, we decided to investigate this rare condition (3
out of 750 melanoma patients in our series). The purpose
of our present study was to systematically review the
literature in order to determine to what extent SLNB or
ALND may alter lymphatic drainage and if a second
SLNB could be considered reliable in this particular on-
cological setting.
2. Materials and Methods
A web search (Ovid Medline®) was conducted over the
last 10 years with following medical subject headings:
sentinel lymph node biopsy, breast neoplasms, melanoma,
second (title word), lymphatic anatomy and axilla. Fol-
lowing identification of publications of interest, this
search was completed by Medline tools using “similar
references” or “citing references”. Case reports (1case)
were discarded and some of these have been previously
collected by Palit et al. [10]. Following data have been
extracted: first axillary dissection (SLNB or ALND),
success rate for second SLNB, number of patients and
detailed sites for extra-axillary SLNB, rates of metastatic
SN (sentinel node) and length of follow-up when avail-
able. All these data are summarised in Table 1. Other
data were reviewed such as: definition of SN and proto-
col for the SN anatomopathological examination.
3. Results
Our literature research totalizes 523 patients in 17 dif-
ferent studies, which included between 2 and 117 pa-
tients each (Table 1) [9,11-26]. Overall SN was succes-
fully detected in 365/523 patients (70%). Extraaxillary
SLNB was encountered in 114/365 patients (31%). This
figure was quite variable throughout studies as all extra-
axillary SN were not systematically searched for in all
studies (especially internal mammary) despite the fact
that there was a significant number of metastatic extra-
axillary SNs. Extra-axillary locations included internal
mammary, intramammary, interpectoral, parasternal,
infraclavicular and cervical in. All these location have
already been observed in primary SLNB for breast can-
cer [27]. Keeping in mind that SNs were not all removed,
we can acknowledge 46 an d 13 patients with axillary and
non-axillary metastatic SNs respectively. Clear definition
for SN was scarce, triple technique for SLNB was not
always the rule: blue dye was not systematically used in
some series. Complete SNs analysis with H.-E. and im-
munohistochemistry were performed in all but three
studies [14,19,22]. A follow-up was available in half of
the studies. No axillary recurrence was observed within a
follow-up period ranging from 15 to 46 months.
4. Discussion
Our literature analysis shows data heterogeneity and lack
of standardization of the various strategies. Despite this,
our review suggests that SLNB after previous radical
lymph node dissection in the same region is surgically
feasible and seems oncologically to be reliable regarding
the evaluation of potential lymphatic spreading of tumour
cells. Lymphoscintigraphy should be regarded as the best
examination tool for highlighting lymphatic anatomy and
actual lymphatic drainage following a previous lympha-
tic dissection in the same regional lymphatic network.
Lymphoscintigraphy shows definitively basin(s) where a
SLNB must be performed, especially for trunk melanoma,
where drainage is frequently unpredictable [28].
The 17 reviewed publications (Table 1), have to be
compared with caution because of several limitations: 1)
heterogeneity of series due to different kind of initial
breast surgery (benign and malignant disease with past
SLNB, ALND or no axilla surgery), 2) blue dye injection
was not systematically performed, and different injection
technique (peritumoral, intratumoral, subcutaneously)
were used, 3) no systematic ALND performed in case of
SLNB failure, 4) variability of nodes detection rate dur-
ing lymphoscintigraphy, 5) number of SNs retrieved and
number of patients, 6) lack of follow-up in order to con-
firm oncological value of second SLNB, among others.
A negative SLNB in breast cancer exposes to 0.3%
axillary recurrence only, within a median delay of 20
months (range 4 - 63) [29]. So the follow-up reported in
table 1 (range 15 - 46) could be an element for assessing
that false negative results after second SLNB were con-
ALND, which was a common procedure in patients
with breast cancer in the past, is now replaced b y sentin el
lymph node dissection as a validated staging procedure.
It is generally accepted that a micrometastatic disease in
sentinel nodes does not oblige to perform ALND in pa-
tients with breast cancer, while it is still a debated matter
in melanoma patients. SLNB following previous breast
and axillary surgery is another matter of debate. The
number of metastatic lymph nodes is in parallel with the
mean number of lymph nodes retrieved during a radical
lymph node dissection. This mean number can be con-
Open Access JCT
Axillary Sentinel Lymph Node Biopsy for Breast Cancer and Melanoma Patients after Previous Axillary Surgery:
A Systematic Review
Open Access JCT
Table 1. Review of literature for second SLNB after previous SLNB and/or ALND.
Year, author
N (first
N success
for second
rate %
IM Axillary
(i: ipsilateral/
c: contralateral)
(i: ipsilateral/
c: contralateral)
Patients with
positive SN
Ax. +
2004, Sood [11] 4 (4/0) 4 100 4 20i/1c - 2b 1 + 0 NA
2005, Dinan [12] 16 (2/14) 11 69 7 14i/3c 2i/1c 1b
1c 0 NA
2005, Agarwal [13] 2 (0/2) 2 100 2 -1i/2c 0 + 1 25 and 14/0
2006, Newman [1 4 ] 10 (1/7) 9 90 7 32i/7c - - 0 NA
2006, Roum e n [1 5] 12 (2/10) 10 83 7 36i/4c - 2i 3 + 2 24/0
(negative SN)
2006, Taback [16] 15 (11/9) 11 73 5 25i/3c 1i 2f 2 + 1 41/0
2007, Port [9] 117 (54/63) d64 55 19 1152i/5c 1i 1e
3b 8 + 2 26.4/0
2007, Intra [17] 65 (65/0) 63 97 5 463i/0c 1i - 6 + 1 45.9/0
2007, Barone [18] 19 (7/12) 16 84 NA 16i 2 + 0 15/0
2008, Koizumi [1 9 ] 31 (3/16) h 29 94 12 517i /7c - - 1 + 3 NA
2008, Schrenk [20] 30 (13/13) g19 63 5 415i /1c - 1f 4 + 0 NA
2008, Cox [21] 56 (56/0) 45 80 1 145i/0c - - 9 + 0 NA
2008, Axelsson [22] 47 (1/43) l 20/44 45 7 3l24i/1c 2i 2i 7 NA
2008, Karam [23] 20 (4/11) j 13 65 2 115i/0 c 1i - 2 + 0 NA
2009, Tasevski [24] 18 (3/15) 12 67 9 55i/5c - - 0 + 3 NA
2010, Van
der Ploeg [25] 36 SLNB k
12 ALND k26
6 72
50 17/26a
5/6 10
3i/4c -
- 5e 2f
3b ?k
2 39/0k
2010, Derkx [26] 13 (13/0) 5 38 NA -5i - - 1 + 0 13/0
Overall 523 365 70 114/365
46 + 13
SLNB: previous sentinel lymph node biopsy. ALND: previous axillary radical lymph node dissection. IM: internal mammary. Other extra-axillary SNs: bin-
tramammary, ccervical, einfraclavicular, finterpectoral, iclose to side of recurrence. NA: not assessed. ameans any SN outside ipsilateral axilla, patients had
drainage to more than one basin (sometimes difficult to distinct number of nodes and number of patients). d115 patients: 2 had bilateral breast carcinoma. g 1
patient had a previous axillary benign tissue resection and three melanoma surgery. h10 patien ts received radi otherapy to br east and axilla and 12 patients had
breast su r g ery only. j1 patient had bilateral breast cancer, 5 patients had breast surgery only. kout of a series of 115 patients including previous breast surgery for
benign pat hology, ov erall 12 p atients out of 115 h ad positive S N. l3 patien ts had a lu mpectomy on ly and 3 wer e exclud ed because n o blue dye was used. Int er-
nal mammary SN were not.
sidered as quality control surrogate marker in ALND.
The median number of analysed lymph nodes was 13
(range 1 - 51) in a large retrospective study on 31,679
breast cancer patients [30]. There are important differ-
ences in ALND in breast cancer or in melanoma. So a
complete lymph node dissection has the not the same
magnitude in breast cancer (usually limited to lev el I and
II) when compared to melanoma (usually including level
I to III). This may partly explain the possibility to per-
form SLNB after previous “radical axillary dissection” in
breast cancer patients. In melanoma patients ALND is
regard ed as a therapeutic proced ure and as such it results
in harvesting more lymph nodes than in breast cancer
patients [31,32]. Redo ALND following previous ALND
for breast cancer should be performed if necessary, be-
cause it may yield a similar or even a higher number of
nodes compared with prev ious initial ALND [18].
5. Comprehensive Anatomy of Lymphatics
of the Upper Limb Trunk and Axilla
Comprehensive reviews of upper limb and upper torso
and breast lymphatic anatomies showed that lymphatics
converge to a dominant axillary lymph node with nu-
merous connexions to defined territories along the limb
[33-35]. Some studies have observed that in SLNB for
breast cancer, dermal and parenchymal lymphatics drain
to the very same axillary node(s) [36], but lymphatic
watershed in the breast does exist, thus explain ing physi-
ologic extra-axillary drainage. Based on Suami’s study,
peritumoral dye/radiocolloid injection should be pre-
ferred [37]. There is often more than one first-tier node
[37]. Lymphatic drainage of the upper limb may rarely
Axillary Sentinel Lymph Node Biopsy for Breast Cancer and Melanoma Patients after Previous Axillary Surgery:
A Systematic Review
bypass level I and II of the axilla by using the way
through lymphatics along cephalic vein and may drain
directly in level III (infraclavicular fossa) [38]. This was
already described in Sappey’s drawings [33]. There are
some connexions between superficial and deep lymphatic
network [33], these may also account for interval sentinel
nodes [38]. Of note, opening of lymphatic connections
between deep and superficial network may prevent lym-
phedema after complete axillary dissection [39]. Varia-
tion in lymphatic vessels anatomy was illustrated by
Wall et al. in patients with SLNB for trunk and extremi-
ties melanoma: this group showed that 30.5% of patients
had multiple lymphatic channels draining to a single ba-
sin, while 58.8% had one single lymph channel only
identified from the primary tumour site [40].
6. To What Extent Previous Surgery and
Lymphatic Dissection (SLNB or ALND) in
the Axilla Would Change the Lymphatic
Network and the Success for Second
Luini et al. showed that a previous breast biopsy would
not modify SLNB accuracy in a study with 543 breast
cancer patients and a 99% SN identification rate [41]. In
70 breast cancer patients with previous breast augmenta-
tion or reduction surgery, SNs were identified in all and
were positive in 32%. Only one patient had bilateral
axillary drainage and ipsilateral in ternal mammary drain-
age [42]. In another study, axillary SNs were seen in the
axilla in 100% of patients following plastic surgery and
in 91% after excisional biopsy only [25].
Table 1 shows that mean success rate for second
SLNB was 70% (45% - 100%) and was clearly related to
previous axilla surgery in the larger series where sub-
groups were analysed: 38% after ALND and 74% after
SLNB in Port’s study [9], 50% and 72% respectively in
van der Ploeg’s study [25]. Schrenk et al. observed a
63% successful SN detection rate, which correlated with
a positive lymphoscintigraphy and less than 10 nodes
removed during the first axillary surgery [20]. Axelsson
et al. observed however that success for second SLNB
was not related to the number of lymph nodes at first
surgery [22].
Compared to radical lymph node dissection, SLNB
shows significantly a lower risk for lymphedema: in
4.6% - 16% for ALND patients and 0.3% - 5% for SLNB
patients [43-45]. Lymphedema definition and measure-
ment may vary, but there is a significan tly increased risk
with higher body weight, infection and injury after sur-
gery [45]. Despite removal of a central key node or
nearly all nodes, existing complex lymphatic network,
accessory lymph channels or regenerated lymphatics may
explain the fact that many patients did not experience
lymphedema following a first axillary dissection [39].
Lymphedema risk following second axillary dissectio n is
unfortunately not reported in the reviewed papers in Ta-
ble 1.
Fibrosis has been proven in an animal model as a key
inhibitor in lymphatic regeneration. Extent of surgery or
reg io n al morbidity (lymphocele infection or lymphang itis )
may explain why lymphatic anatomy is altered to various
degrees [46]. Moreover, radiation and chemotherapy may
also play a negative role in SN detection. Axillary dis-
section followed or not by radiotherapy may alter lym-
phatic drainage so that anterior chest may drain directly
to internal mammary nodes [47,48]. Xing’s meta-analy-
sis showed that SLNB was still reliable following induc-
tion chemotherapy alone in breast cancer patients [49].
Some authors have observed that neither adjuvant radio-
therapy [9,17,21] nor chemotherapy [9] affect SN identi-
fication rate. Failures may also be explained by alteration
of radiotracer detection by a change in lymphatic net-
work (diffuse small lymphatics) due to fibrosis or be-
cause of an enlarged metastatic lymph node. One study
observed blue dye failure in 9/11 patients [12] and an-
other observed that only 50% SNs were blue while 89%
were hot [9], thus justifying the use of both tracer meth-
One interesting fact in table 1 is the proportion of 31%
of extra-axillary SNs (15% - 100 %) observed during sec-
ond SLNB. This figure is in accordance with 6% - 33%
reported in the literatu re for first SLNB [9,25,27]. Extra-
axillary SNs were more frequently observed after ALND
(60% - 84%) than after SLNB (14% - 65%) at first sur-
gery [9,20,25]. These were mainly IM and contralateral
axilla, many times following ALND at first surgery.
Surgery for extra-axillary SN is more demanding due to
the need for internal mammary nodes and scary tissues
dissection for example [9,20,50].
In case of successful second SLNB, reliability of sec-
ond SLNB was demonstrated eith er by 1) follow-up with
negative axillary/extra-axillary recurrence, 2) by axillary
dissection in patients with non-metastatic SN at second
SLNB or 3) in patients where second SLNB failed. With
a median follow-up of 45.9 months, Intra et al. did not
observe any axilla recurrence in the 57 patients who had
no further ALND after negative SLND [17]. Dinan et al.
[12] had one single patient with SLNB at first surgery
and negative SLNB at second surgery: a further ALND
showed 14 negative nodes. In Schrenk’s study, 13 pa-
tients out of 15 who had negative SN had a further
ALND, which showed no other metastasis in a mean of
14.3 nodes (5 - 24), with a false negative rate of 0% [20].
Karam et al. chose to perform complementary ALND in
11 patients with successful second SLNB only in 4 pa-
tients who had SLNB at first surgery: none had positive
Open Access JCT
Axillary Sentinel Lymph Node Biopsy for Breast Cancer and Melanoma Patients after Previous Axillary Surgery:
A Systematic Review 1399
nodes [23]. Port et al. removed additional non-SN in 23
out of 54 patients with successful reoperation with nega-
tive SN: one patient had positive internal mammary SN
and the other a palpable positive non-SN [9]. Overall
sensitivity and false negative rates were difficult to as-
sess based because of incomplete data from table 1.
Concomitant/sequential melanoma and breast cancer is
indeed a rare event but was already described by Sood in
2004 (1 patient out of 4) [11] and by Schrenk in 2008 (3
out of 30) [20]. Collision tumours (SN with two his-
tologically different metastatic deposits) with breast
cancer and melanoma had a 0.5% incidence (52 cases in
20 years) at The Moffitt Cancer Centre [51]. Simultane-
ous neoplasms with only one of them detected can ex-
pose either to collision tumour or destruction of lympha-
tic pathways leading to a second metastatic undetected
SN. In case of breast cancer a median delay of 20 months
[29] would be necessary and only weeks for melanoma in
order to observe a clinically or radiologically enlarged
lymph node.
7. What Should Be the Next Step for Patients
Who Failed Second SLNB Detection?
According to previous detection (SLNB or AL ND) some
authors propose surveillance [23]. Intra et al. detected
positive nodes in one single such patient with a PET-CT
[17], majority of authors propose in selected patients an
ALND, who revealed positive nodes in 1/11 patients [19],
1/2 patients (out of 11 failures) [21], 2/3 patients (out of
7 failures) [23]. In the study of Port et al., 53 patients
with failed second SLNB 29 had no further additional
nodes and one patient out of 24 ALND (1-26 further
nodes) had a metastatic lymph node [9]. Secondary ALND
after a previous ALND is able to remove 0 - 16 further
lymph nodes [12,16,18,20].
8. Conclusions
Based on this comprehensive literature review, definitive
conclusions are difficult to draw because of the rare con-
dition, and because of the retrospective nature of the
studies, the lack of complete survival data and data het-
erogeneity. Patients with a second malignancy are also
usually excluded from randomized trials. However, fol-
lowing conclusions can be proposed:
1) Previous axillary dissection (SLNB or level I-II
lymph node dissection for breast cancer) does not pre-
clude a new SLNB (feasible in 70%) and completion of
ALND when positive SNs are detected. Even in more
radical surgery for melanoma patients, SLNB would be
able to detect where the actual lymphatic flow has been
2) Due to multiplicity of unusual drainage way, clas-
sical triple technique of lymphatic mapping should be
recommended, associating lymphoscintigraphy (dyna-
mic/static), blue dye injection and intraoperative use of
hand held gamma probe. Of note, SLNB rules must be
respected: remove all enlarged su spicious non SN.
3) In this setting when detected, extra-axillary SNs
should be dissected as they may be the only SN and the
only metastatic SN. Internal mammary SLNB is a stan-
dardized procedure [27,31,47,50]. It is however impossi-
ble to say if ALND can be avoided when only an extra-
axillary SN is positive, in the same way as in a first
SLNB [50].
4) In case of successful second axillary SLNB with
negative SN and in case of extra-axillary SLNB with
negative SN, the absence of recurrence in the present re-
view indicates that avoidance of complementary ALND
is a safe option.
5) Complementary ALND should be discussed in case
of failed second SLND. At least a strict follow-up com-
bined with echography, CT-scan or PET-CT should be
6) Complementary ALND should be discussed when
SLNB is positive (regardless of previous ALND or
SLNB) and in contralateral axilla in case of positiv e con-
tralateral positive SN.
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SN: sentinel lymph node;
SLNB: sentinel lymph node biopsy;
ALND: axillary radical lymph node dissection.