European Journal of Cancer 204 (2024) 114049

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European Journal of Cancer

journal homepage: www.ejcancer.com

A selective anatomically based lymph node sampling can replace a side

specific pelvic lymphadenectomy in endometrial cancer with failed sentinel
node mapping
Michele Bollino, Barbara Geppert, Celine Lönnerfors, Jan Persson *
Department of Obstetrics and Gynaecology, Division of Gynaecologic Oncology, Skåne University Hospital Lund, Lund University Faculty of Medicine, Department of
Clinical Sciences, Obstetrics and Gynaecology, Lund, Sweden

A R T I C L E I N F O A B S T R A C T

Keywords: Aim: To evaluate the locations of metastatic pelvic sentinel nodes (SLN) and the proportion of SLNs outside and
Endometrial cancer within defined typical anatomical positions along the upper paracervical lymphatic pathway (UPP).
Side specific pelvic lymphadenectomy Patients and methods: Consecutive women with endometrial cancer (EC) of all risk groups underwent pelvic SLN-
Anatomically based sampling
detection using cervically injected indocyanine green (ICG). A strict anatomically based algorithm and defini­
Typical positions of sentinel lymph nodes
tions of SLNs was adhered to. The positions of ICG-defined SLNs were intraoperatively depicted on an anatomical
chart. All SLNs were examined using ultrastaging and immunohistochemistry. The proximal third of the obtu­
rator fossa and the interiliac area were defined as typical positions. The parauterine lymphovascular tissue
(PULT) was separately removed. The proportions of metastatic SLNs, overall and isolated, typically, and atypi­
cally positioned were analyzed per woman.
Results: A median of two (range 1–12) SLN metastases along the UPP including the PULT were found in 162
women. 41 of 162 women (25.3 %) had isolated metastases in the obturator fossa harboring 49.1 % of all SLN
metastases. Three women (1,9 %) had isolated PULT metastases. SLN metastases outside typical positions were
identified in 28/162 women (17.3 %); isolated metastases were seen in seven women (4.3 %), so 95.7 % of pelvic
node positive women had at least one metastatic SLN located at a typical position.
Conclusion: A selective removal of lymph nodes at typical proximal obturator and interiliac positions and the
PULT can replace a full side specific pelvic LND when SLN mapping is unsuccessful. The obturator fossa is the
predominant location for metastatic disease.

1. Introduction option for SLN detection in EC patients [10–14]. Three prospective

Lymph node metastases is a prognostic factor that guides the need for
adjuvant treatment in women with endometrial cancer (EC) [1,2]. Prior
to the introduction of sentinel node (SLN), evaluation of lymph nodes
entailed a full pelvic and paraaortic lymphadenectomy (LND). Due to
the associated risk of lymphatic complications, lymph node assessment
was limited to women with presumed high-risk tumors although erro­
neous preoperative risk group allocation was reported in up to 20 % of
presumed low-risk patients [3–5]. Whether a LND is purely diagnostic or
leads to a survival benefit remains unclear. SLN detection aims to reduce
surgical trauma and postoperative complications while retaining, or
even improving, information on nodal involvement [6–9]. Cervical in­
jection of indocyanine green (ICG) has been shown to be the superior
studies (FIRES, SHREC and SENTOR) demonstrated the potential of an
ICG-based SLN-concept in EC with a pooled sensitivity to detect pelvic
nodal metastases of 95.7 % (95 % CI, 90.2–98.6) [8,15,16]. The SHREC
study, performed in high-risk EC was based on studies on lymphatic
anatomy and utilized a defined anatomically based algorithm, and a
strict definition of SLNs as defined below. Even though reinjection of
ICG was introduced in case of non-mapping, around 10 % of women still
had insufficient mapping along the UPP [8,17]. A parallel study on
low-risk EC patients demonstrated a 16-fold reduction of symptomatic
lower limb lymphedema and a 5-fold decrease in pelvic lymphoceles
when comparing SLN removal only to women in whom a full LND was
performed [18]. Based on these results, the Swedish guidelines from
2020 recommend utilizing the SHREC SLN-algorithm in all EC patients

* Correspondence to: Department of Obstetrics and Gynaecology, Skåne University Hospital, SE-221 85 Lund, Sweden.
E-mail address: jan.persson@med.lu.se (J. Persson).

https://doi.org/10.1016/j.ejca.2024.114049
Received 20 February 2024; Received in revised form 26 March 2024; Accepted 4 April 2024
Available online 12 April 2024
0959-8049/© 2024 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
M. Bollino et al.
deemed fit for adjuvant treatment. In 2021, ESGO included a high
proportion of SLN detection as a quality indicator in EC surgery [19].
Although the lower paracervical pathway (LPP) has been less exten­
sively studied, the SHREC study identified isolated metastases along the
LPP only in non-endometroid EC, thereby recommending restricting
lymphatic dissection to the upper paracervical pathway (UPP) in women
with endometrioid EC [8].
Frequently used algorithms and the ESGO recommend a full side
specific pelvic LND in case of non-mapping [19,20]. Particularly, in
low-risk EC patients this would entail an undesirable increased risk of
lymphatic complications.
The aim of this prospective study was to investigate the overall lo­
cations of metastatic pelvic sentinel nodes (SLN) and the proportions of
isolated metastatic SLNs inside and outside defined typical anatomical
positions along the upper paracervical lymphatic pathway (UPP) to
evaluate whether selective sampling could be a safe option to a side
specific LND in case of non-mapping.
2. Material and methods
Data on mapping rates and anatomical positions of SLNs and meta­
static pelvic SLN in consecutive women with EC undergoing robotic
surgery using the da Vinci Si or Xi system (Intuitive Surgical inc., Sun­
nyvale, CA, USA) was extracted from two prospective non-randomized
trials; the SHREC- trial (clinicalTrials.gov NCT02690259) and an
ongoing parallel “SLN only” study (clinicalTrials.gov NCT03680833)
[8]. Inclusion and exclusion criteria are described in the online study
protocol. The SHREC study included women with presumed high-risk EC
undergoing a pelvic SLN procedure followed by a full pelvic and
para-aortic lymphadenectomy [8]. The “SLN-only study” initially
included women with presumed low-risk EC, and from June 2019 when
the SHREC study was published, all women with EC regardless of pre­
operative risk group. We excluded 56/257 (21.8 %) of women included
in the SHREC study who had undergone surgery at the second partici­
pating institution. The studies were approved by the Institutional Re­
view Board (DNR 2013/163 and 2018/541). All included women gave
LEFT
Obturator fossa
(A)
83/342 (24.3%)
Interiliac area
(B)
54/342 (15.8%)
Lateral external/
distal common
iliac (C)
8/342 (2.3%)
PULT (D)
15/342 (4.4%)
Presacral area
(E)
24/218 (11%)
Fig. 1. Anatomic distributions, and proportions per compartments, of all metastatic pelvic sentinel lymph nodes in endometrial cancer.
Presacral proportions calculated on women with detection of SLNs along the UPP and the LPP
2
European Journal of Cancer 204 (2024) 114049
their written, informed consent. To ensure conformity and adherence to
protocol, the procedures were at first performed by either one of three
experienced (>100 robotic procedures prior to study start) surgeons at a
single institution from June 2014 to October 2023. The main surgeon
responsible for the algorithm and study protocols (JP) initially super­
vised the two additional surgeons. From September 2017, two more
surgeons were gradually introduced, in all cases supervised by the pre­
vious surgeons. A previously published anatomically based SLN algo­
rithm was adhered to identifying SLNs along the upper paracervical
pathway (UPP) in all women, and along the lower (presacral) para­
cervical pathway (LPP) in select women with high risk histologies/cri­
teria [12]. At the onset of surgery, 0.25 ml (2.5 mg/ml solution) of
indocyanine green (ICG) was injected submucosally into the cervix at
2–4–8–10 o′clock respectively [17]. Prior to finalizing the SHREC study,
half the volume was injected into the cervical stroma. The Fire-Fly®
mode of the robotic system was used for visualization of lymphatic
pathways and SLNs. If no mapping occurred along a major pathway
within 10 min observation time, an ipsilateral re-injection of 0.25 ml
ICG-solution was performed submucosally at 3 or 9 o′clock. In order to
identify all lymphatic vessels from the uterus to lateral pelvic nodes, the
retroperitoneal avascular pararectal and paravesical planes were care­
fully developed by the aid of the FireFly mode preserving the lymphatic
vessels and the parauterine lymphovascular tissue (PULT) [17]. Indi­
vidual lymphatic vessels were then identified to define SLNs before any
nodal dissection. A SLN type 1 was defined as the juxtauterine
ICG-positive node with an afferent lymphatic channel with particular
attention to possible parallel lymphatics in the UPP to the obturator,
external iliac and distal common iliac areas. Examples of parallel lym­
phatics are outlined in Fig. 1. In the absence of any ICG positive nodes
along a major pathway, a SLN type 2 (itself ICG negative) was defined by
an ICG-positive afferent lymphatic channel ending in that node. Any
macroscopically suspect nodes, regardless of ICG uptake, were defined
as “SLN-macro” (defined as ICG positive or ICG negative). The PULT was
removed separately and processed as SLN-tissue. The PULT, described in
a previous publication, including an online video of the surgical steps of
its removal, and further explained by Bizzarri et al, is usually stained
RIGHT
Obturator fossa
(A)
85/342 (24.8%)
Interiliac area
(B)
39/342 (11.4%)
Lateral external/
distal common
iliac (C)
7/342 (2.1%)
PULT (D)
9/342 (2.6%)
Presacral area
(E)
18/218 (8,3%)
M. Bollino et al.
with ICG as a whole and represents the distinct lymphatic tissue con­
necting the uterus with lateral pelvic nodes, hence different from a full
parametrectomy [21,22]. Abiding by the results from the SHREC study,
after June 2019, SLN detection along the LPP was only performed in
women with non-endometrioid EC. Due to longitudinal variations of
positions of SLNs and cross-over between sides, typical anatomic posi­
tions along the LPP cannot be defined. In case of non-mapping a full
presacral lymphadenectomy was performed and all retrieved nodes
processed by US and IHC for a uniform comparison on the risk of nodal
metastases with ICG-based SLNs. Intraoperatively, an anatomical chart
was completed by the consol surgeon where position and type of SLNs
were described. A standardized chart with defined SLN positions,
including types of SLNs with corresponding prelabelled jars, accompa­
nied the pathology report (online Study Protocol). Typical positions
were defined as the “proximal obturator fossa” (the proximal third of the
obturator fossa, lateral of the obliterated umbilical artery, dorsomedial
of the ventral rim of the external iliac vein, ventral of the obturator
nerve) and the “interiliac position” (lateral of the obliterated umbilical
artery, ventromedial of the external iliac vein, within the bifurcation of
the external and internal iliac arteries). These positions are reached by
exploring the “lateral paravesical and pararectal spaces” [21]. External
iliac SLNs lateral of the external iliac artery, regardless of longitudinal
position, and nodes located in the distal 2/3 of the obturator fossa were
considered atypically positioned (Fig. 2). All SLN-tissues were
embedded and bisected if the minimum thickness exceeded three mm.
Ultrastaging using hematoxylin and eosin staining (H&E) was performed
in five sections at three different levels; 200 µm apart if the maximum
diameter of the SLN tissue exceeded one mm. Immunohistochemistry
(IHC) with staining for pan-cytokeratin and cytokeratin MNF 116 was
performed. Non-SLNs with a thickness of less than three mm were
embedded entirely and for nodes exceeding three mm at least half the
Fig. 2. Schematic view illustrating typical (A,B) and examples of atypical (C,D)
positions of sentinel lymph nodes along the Upper Paracervical lymphatic
Pathway (outlined dark). A. Typical proximal obturator position: SLNs located
within the proximal third of the obturator fossa, ventral of the obturator nerve,
lateral of the obliterated umbilical area and dorsomedial of the ventral rim of
the external iliac vein. B. Typical interiliac position: SLNs located within the
bifurcation of the external and internal iliac arteries, lateral of the obliterated
umbilical artery and ventromedial of the external iliac vein. C. Example of an
atypically positioned obturator SLN located in the distal 2/3 of the obturator
fossa. D. Example of atypically positioned external iliac SLN located lateral of
the external iliac artery.
3
European Journal of Cancer 204 (2024) 114049
node was embedded. Non-SLNs were stained for H&E but were not
subjected to IHC. Metastatic disease was classified according to a
modification of the American Joint Committee on Cancer staging defi­
nitions for axillary nodes in breast cancer (Macro-metastases = tumor
greater than 2.0 mm in diameter, Micro-metastases = tumor cell ag­
gregates between 0.2 and 2.0 mm in diameter, Isolated tumor cells =
individual tumor cells or aggregates that are less than 0.2 mm in
diameter and less than 200 cells) [23]. Data from the intraoperatively
used charts and study protocols was continuously transferred to a
research file used for the analysis. The mapping rates among all women
and the pelvic node positive women were calculated. In addition, the
proportion of ICG-mapped metastatic SLNs and their anatomical posi­
tion within the UPP including the PULT were investigated.
3. Results
1218 women were screened, 1103 were enrolled, and after exclu­
sions, data from 1060 women with at least one ICG-positive node along
the UPP including the PULT were included in the final analysis (Fig. 3).
As perceived intraoperatively by the surgeon per definitions, a median
of four (range 1–8) ICG defined SLNs were retrieved along the UPP of
which 96.0 % were Type 1 % and 4.0 % Type 2. Defined by final his­
tology, a median of two (range 1–12) ICG-defined metastatic SLNs were
identified along the UPP in 162 women. Detailed demographic and
clinical data for node positive women is outlined in Table 1. For all
included women, bilateral mapping rate in the UPP was 91.9 %, uni­
lateral mapping was 5.4 %, and the non-mapping rate was 2.7 %. The
162 women with ICG-defined pelvic SLN metastases mapped bilaterally
in 87.6 % and unilaterally in 12.4 %. Incomplete mapping was more
common in pelvic node positive women (20/162, 12.3 % compared with
37/898, 4.1 %, p < .001). There was no difference in mapping between
the left and right UPP (94.6 % compared with 95.2 % respectively,
p = .51). In the 162 women with SLN metastases along the UPP, the
external iliac area had a higher mapping rate than the obturator fossa
(92.3 % vs 76.3 %; p < .001) and a higher rate of atypically positioned
SLNs (14.9 % vs 4.9 %) although the obturator fossa harbored isolated
metastases in 25.3 % of women and contained 49.1 % of all SLN me­
tastases. The PULT contained metastatic nodes in 22 of 162 (13.6 %)
women; three (1.9 %) of which had isolated PULT-metastases. In women
with non-endometrioid histology, isolated metastases along the LPP
were identified in 2/53 (3.8 %) of node positive women. Paraaortic
metastases was present in 31/219 (14.2 %) high risk women with an
upfront paraaortic dissection and in 44.9 % of women with metastatic
pelvic SLNs. Isolated paraaortic metastases were found in 3/153 (1.9 %)
SLN negative women. Details and locations of metastatic SLNs, all and
isolated are outlined in Fig. 1 and Table 2. In all, 95.7 % women had at
least one ICG-defined typically positioned metastatic SLN along the UPP
(including the PULT).
4. Discussion
Of node positive women with EC, 95.7 % had at least one typically
positioned metastatic ICG defined SLN along the UPP including the
PULT suggesting that select removal of nodes at these positions can
replace a full side specific LND in case of non-mapping. This is partic­
ularly valid in women with low-risk EC in whom reducing the extent of
lymph node dissection and associated lymphatic complications while
retaining a high detection rate for metastatic disease is key. The high
proportion of SLN-ICG defined node positive women indicated by this
study to be identified by select removal of nodes at defined typical po­
sitions is due to a low rate of isolated SLN metastases outside typical
positions. The results underline the importance of exploring for parallel
lymphatics within the UPP. Even though the interiliac position is more
frequently mapped, the high rate of isolated metastases in the obturator
fossa underlines the importance of exploring this area even if it is more
difficult to access. In fact, the significantly overall lower ICG-based SLN
M. Bollino et al. European Journal of Cancer 204 (2024) 114049

Fig. 3. Strobe flow chart of consecutive women with endometrial cancer assessed for eligibility for a prospective study evaluating positions of metastatic pelvic SLNs
per defined anatomical positions.

4
M. Bollino et al. European Journal of Cancer 204 (2024) 114049

Table 1 Not removing the PULT would have left another 1.9 % of node
Clinicopathologic characteristics of 167 node positive women with endometrial positive women undetected. Removal of the PULT was in our series not
cancer, planned for robotic hysterectomy and detection of pelvic sentinel lymph associated with any surgical complications and added an approximate
nodes lymph node (SLN), using cervically injected Indocyanine green as tracer. 3–5 min to the procedure. Whether a removal of the PULT should be
Variable n (%) or median (range) as appropriate included in a general SLN algorithm in endometrial cancer may be a
Age (years) 72 (41–89) matter of debate, potentially restricting removal of the PULT to women
Body mass index (kg/m2) 28.0 (16.6-47.5) with an estimated higher risk for nodal metastases. Outside the primary
ASA aim of this paper, added for information, 3.8 % of node positive women
I 21 (12.6 %) with non-endometrioid histology had isolated presacral nodal metasta­
IIa 146 (87.4 %)
Final histology
ses (LPP) suggesting a customized SLN-algorithm. Isolated paraaortic
Endometrioid adenocarcinoma FIGO grade I-II 92 (55 %) metastases were identified in 1.9 % high risk women which is lower than
Endometrioid adenocarcinoma FIGO grade III 22 (13.2 %) previously reported, logically due to an increased proportion of small
Serous adenocarcinoma 30 (18 %) volume pelvic metastases diagnosed by US and IHC, an additional
Clearcell adenocarcinoma 10 (6 %)
strength of the SLN concept [24].
Carcinosarcoma 10 (6 %)
other 3 (1.8 %) The bilateral mapping in this study was 91.9 % in all patients, and
Stage (Figo 2009) 87.6 % in women with SLN-metastases. The SENTOR study had a
III C1 123 (73.6 %) bilateral mapping rate of 77.7 % and the FIRES study had a bilateral
IIIC2 44 (26.4 %) mapping rate of 52 %, where the latter, but not the former, allowed for
Final uterine stage (irrespective of overall surgical
reinjection [15,16]. These results underline a need for an alternative
stage)
Ia 59 (35.3 %) approach to a full side specific lymphadenectomy to minimize lymphatic
Ib 108 (64.7 %) complications in case of non-mapping. Mapping is likely dependent on
II 29 (17.3 %) overall surgical experience, injection technique, volumes and concen­
Operative timeb
trations of the utilized ICG solution. Despite the higher mapping rates,
Hysterectomy + SLN (UPP) 71 (37-202) 68 (37-136)
Hysterectomy+ SLN(UPP+LPP) 105 (90-150) 82 (56-193) we believe this study does not provide evidence on details for injection
Hysterectomy+ SLN(UPP+LPP)+ pelvic LND 184 (153-191) 123 (63- of ICG.
161) Adhering to a strict protocol and definitions of SLNs and using
Hysterectomy+ SLN(UPP+LPP)+ pelvic and 218 (145-440) 169 (102- standardized charts to prospectively depict anatomical locations and
infrarenal LND 342)
type of SLNs is unique and a strength of this study. In addition, the study
Estimated blood loss 50 (0-1200)
Conversion to laparotomyc 2 (1.2 %) has a high degree of internal validity due to a single center setting and a
Surgical lymph node assessment limited number of experienced surgeons with pooled case load of more
SLN biopsy only 100 (59.9 %) than 1300 SLN-procedures. To generalize the results, surgical skill and
SLN + Pelvic LND 16 (9.6 %)
strict adherence to protocol is a prerequisite underlining the importance
SLN + Pelvic + LND to the inferior mesenteric artery 6 (3.5 %)
SLN + Pelvic + infrarenal LND 45 (27 %)
of centralized cancer care. Even so, due to a less distinct longitudinal
Number of SLNs as perceived by surgeon 4 (1–8) limit in the obturator fossa, an interpersonal fluidity among surgeons
Pelvic lymph node count 26 (8–57) with regards to definition of typical positions might have affected the
Paraaortic lymph node count 13([3–51) results. This weakness is however likely counteracted by the distinct
Women with pelvic LNM along the UPP+ PULT 162 (97 %)
typical position in the interiliac area. The present results are a comple­
Data outside main scope of study
Women with isolated presacral metastasesd 2/53 (3.8 %) ment to, and not a replacement of, use of tracer. Obesity is not un­
Women with isolated para-aortic metastasesd 3/153 (1.9 %) common in women with EC and ICG enables the detection and removal
of a restricted number of nodes embedded in fatty tissue reducing the
ECOG, Eastern Cooperative Oncology Group; PS, performance status; ASA,
American Society of Anesthesiologists; FIGO, International Federation of Ob­ risk of removing an increased number of non-representative nodes, and
stetrics and Gynecology; LND, lymph node dissection; LNM, lymph node me­ also associated complications. This is particularly apparent in the
tastases. UPP: upper paracervical pathway, LPP: lower paracervical pathway. technically more challenging obturator fossa. In elderly women it is not
a
Including ASA class III due to body mass index/comorbidity. unusual with tortuous vessels that complicate an anatomically based
b
Surgical time skin to skin for the first and second cohorts of procedures. sampling. ICG guidance facilitates the detection of SLNs in these patients
c
Conversion after protocol SLN procedure was completed. and also in patients with atypical location of SLNs. However, as an
d
Subgroups included in the overall analysis of SLN metastases along the UPP. incomplete mapping was more common in node positive women; an
anatomical lymphatic sampling as suggested by the present study might
detection rate among node positive women, particularly in the obturator increase detection of metastatic disease.
fossa (harboring 49.1 % of all SLN metastases) may contribute to the In conclusion, nodal metastases were located at typical positions in
concept of an anatomically based sampling as this would entail an the proximal obturator and interiliac area including the PULT in 95.7 %
obligatory removal of nodes at the obturator and interiliac positions. of women with pelvic nodal metastases compared with a successful

Table 2
Schematic overview of the typical and atypical localization of metastatic pelvic SLNs per compartments.
External iliac area Obturator fossa PULT Presacral area

Data as n (%) as appropriate Typical position Atypical position Typical position Atypical position

Proportion of all metastatic SLNs 93/342 15/342 154/342 14/342 24/342 42/342
(27.2 %) (4.4 %) (45 %) (4.1 %) (7 %) (12.3 %)
Proportion of women with metastatic SLN per position 79/162 15/162 114/162 13/162 22/162 20/53e
(48.7 %) (9.2 %) (70.4 %) (8 %) (13.6 %) (38 %)
Proportion women with isolated metastatic SLN per position 24/162 3/162 37/162 4/162 3/162 2/53e
(14.8 %) (1.8 %) (22.8 %) (2.5 %) (1.9 %) (3.8 %)

Compartments presented independently from each other, implying that each patient can have SLN’s in multiple compartments.
e
women with non-endometrioid histology EC.

5
M. Bollino et al.
bilateral ICG defined SLN procedure. This suggests that in case of non-
mapping, a selective removal of nodes in the proximal obturator fossa
and the interiliac position can replace a full side specific pelvic LND. The
expected decreased risk of lymphatic complications is beneficial and
may further accelerate the use of SLN detection also in women with low-
risk EC.
Ethical approval
The study was approved by the Institutional Review Boards (Skåne
University Hospital, Dnr 2013/163 and 2018/541).
Funding
The study was supported by Skåne County Councils’s Research and
Development Foundation (Grant numbers REGSKANE 353601,
REGSKANE 632231 and REGSKANE 43656).
Role of the funding source
The funding sources solely contributed with means for carrying out
of the study but were otherwise not involved.
Trial registration
The SHREC-trial (clinicalTrials.gov NCT02690259) and the “SLN
only“ trial (clinicalTrials.gov NCT03680833).
Declaration of Competing Interest
The authors declare the following financial interests/personal re­
lationships which may be considered as potential competing interests:
Jan Persson have received honoraria for proctoring and lectures from
the manufacturer of the da Vinci system. Celine Lönnerfors have
received honoraria for lectures from the manufacturer of the da Vinci
system. The other authors report no conflicts of interest.
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