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16.4 Clinical Indications
16.4.1 Predictive andPrognostic
Biomarker
[18F]-FES has been demonstrated to distinguish
tumors with intrinsically good or poor prognosis,
alone [35, 36] or in combination with [18F]-FDG
[37–39], and to determine which therapies could
be effective in which patients [35, 37, 38, 40–55].
Measurements of SUVmax of [18F]-FES PET/CT
serial images could be used to predict the patient
progression-free survival (PFS) receiving ER
antagonist therapy, such as fulvestrant [35, 46].
While the combination of [18F]-FES and
[18F]-FDG is shown to be particularly useful in
identifying ER heterogeneity in BC bone metastases, which signicantly associated with survival. Moreover, the extension of the FDG-avid
component correlates with the risk of disease
progression [39]. The most important clinical
impact is the ability of [18F]-FES to predict
patients who can be treated successfully by hormonal therapies. Despite ER+ breast cancer on
IHC, most of the patients respond to rst-line
hormonal therapies, and less than half respond to
second- or third-line hormonal therapies [41].
Only a functional ER able to bind estrogen
ligand, visualizable using [18F]-FES as PET
radiotracer, is a good predictive biomarker [43].
Several studies have demonstrated the predictivity of this radiotracer for selecting patients that
will benet from different kinds of therapies,
such as unspecic hormonal and chemotherapy
[
43] or tamoxifen and hormonal therapies fol-
lowing progression on tamoxifen [44, 45]. Also,
in the case of novel hormonal therapies, such as
SERDs (fulvestrant), which degrade ER and thus
block estrogen binding to ER, aromatase inhibitors (AI), which block estrogen production, and
cyclin-dependent kinase (CDK) 4/6 inhibitors,
which block downstream ER effects, [18F]-FES
seems to be a good predictive biomarker. The
results of Fig.16.6 show how only a three-way
PET classier ([18F]-FES heterogeneous,
Fig. 16.6a, low [18F]-(FES/FDG) and high
[18F]-(FES/FDG) groups, Fig. 16.6b) remained
the only independent, statistically signicant
prognostic factor for PFS (Fig.
with ER-positive metastatic breast cancer under
fulvestrant therapy [56].
16.6c) in patients
16.4.2 ER Assessment
In France, the [18F]-FES is approved for the
whole-body evaluation of recurrent ER-positive
breast cancer in place of biopsy [17]. While the
FDA strongly encourages bioptic conrmation of
[18F]-FES PET ndings, in line with prevailing
practices that biopsy is the best practice for treatment whenever possible (5). However, in the case
of the brain or deep osseous spinal lesions where
the biopsy is difcult, impossible, or only possible with substantial risks, the use of [18F]-FES to
assess a functional ER is very useful. Bonapati
[57] et al. reported how in two representative
cases the use of [18F]-FES PET/CT improves the
detection of intraorbital metastases in ER-positive
BC (Fig.16.7a, b). Abnormal intense [18F]-FES
activity in the right posterior orbit (A, arrow) and
normal physiologic 18F-FDG activity in the right
extraocular muscles (B, arrow). Adopted from
[57].
16.4.3 Problem-Solving Clinical
Dilemmas
In a recent retrospective study, Boers [58] etal.
investigated the value of [
management of clinical dilemmas in BC patients,
not solvable with standard workup. They analyzed 100 scans performed on 83 patients in
Groningen between 2009 and 2019. The clinical
dilemma, as described in Table16.1, was solved
in 87 of 100 scans (87%). Most of the frequency
of solved dilemmas was related to whether scans
were 18F-FES–positive (n=63) or [18F]-FES negative (n=37; P<0.001) rather than to itself clini-
cal dilemma category (P=0.334) [58].
Similar results were reported [59–61] using
[18F]-FES to solve a clinical dilemma in the case
of inconclusive results from other diagnostic
studies. Even if van Kruchten etal. found FES
PET solved clinical problems and led to therapy
18
F]-FES PET in the
278
a
b
Months
https://t.me/med1917
F-FDG
18
M. R. Ruggiero et al.
P < 0.001
Heterogeneous group (n = 12)Low FES/FDG (n = 11)
High FES/FDG (n = 12)
F]-FES/FDG SUVmax (0.96); (c) Kaplan–
18
F]-FES positive metastatic lesions were divided
18
010203040
1. 0
0.8
0.6
0.4
0.2
0.0
c
progression-free survival (proportion)
Meier curves of PFS stratied by the three classications groups. (Adopted and modi-
ed from [56])
group. Patients with 100% of the [
into two groups by the median ratio of [
F-FDG
18
Heterogeneous group
F]-(FES/FDG)
18
F-FES
18
F-FES
18
F-FDG
18
F]-FES.His PFS was 3.7months with any clinical
18
F]-FES positive and negative lesions. The left rib shows signicant
18
F]-FDG but not on [
18
F-FES
18
Low FES/FDG High FES/FDG
uptake on [
Fig. 16.6 (a) Representative cases of a heterogeneous group. A 50-year-old female
patient has both [
benet from fulvestrant treatment; (b) representative cases of the [
ab
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Fig. 16.7 Abnormal intense [18F]-FES activity in the right posterior orbit (a, arrow) and normal physiologic [18F]-FDG
activity in the right extraocular muscles (b, arrow). (Adopted from [57])
279
Table 16.1
performed on BC patients [
The clinical dilemma category was modied
from the original paper [58]
Inability to determine the extent of
metastatic disease or suspected metastatic
disease with the standard workup
Unclear ER status of the tumor 31
Inability to determine which primary
tumor caused the metastases
The clinical dilemma category in 100 scans
58]
Number of
cases
52
17
comparison of the performance of both
radiotracers [18F]-FES PET and [18F]-FDG
PET.Figure16.8 is an example of this comparison [62]. Some studies demonstrated not only
comparable sensitivities [62–64] but also the
change in clinical management in 26% of patients
[64]. A retrospective analysis of six prospective
trials where [18F]-FES and [18F]-FDG PET were
performed in close relation identied patients
with invasive lobular breast cancer (ILC) as a
changes in 48% of patients, the detection of liver
metastases by [18F]-FES PET was poor conrm-
subset of ER-positive breast cancer where FES
PET compared favorably to FDG PET [
ing the biggest issue of the use of FES in clinical
practice [59].
16.4.5 Correlation ER-Targeted
18
Therapeutics and[
F]-FES
16.4.4 Systemic Staging
In the era of improving personalized medicine the
There are ongoing prospective clinical trials of
[18F]-FES PET for the staging of ER-positive
breast cancer in Europe (Clinicaltrialsregister.
EU) and the USA (ClinicalTrials.gov). Current
standard-of-care imaging for systemic staging of
breast cancer is CT/bone scan and the FDG PET/
CT.So, the aim of most ongoing projects is the
use of [18F]-FES PET not only to assess ER blockade in patients on ER antagonists, especially in
patients who fail to respond, but also in the early
stages of drug development is increasing and many
groups reported the success of this paradigm.
In 2011, Linden etal. evaluated estrogen binding
changes in patients with metastatic ER-positive BC
65].
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M. R. Ruggiero et al.
a b
c
d
e
Fig. 16.8 [18F]-FDG and [18F]-FES PET/CT images of a
46-year-old female with lobular carcinoma and histologically conrmed ER-positive recurrence in the left axillary
level II lymph node (Allred score=8). Maximum intensity projection (a) and transaxial [
show equivocal uptake in the left axillary lymph node
18
F]-FDG images (b–e)
after different kinds of endocrine therapy [48], such
as the receptor blocking agents (tamoxifen and fulvestrant) and aromatase inhibitors. The [18F]-FES
SUV (dened as [18F]-FES SUV≤1.5) allowed to
discriminate between complete and uncomplete
tumor ER blockade [48]. Indeed, Van Kruchten
et al. determined the fulvestrant dose needed to
abolish ER binding of estrogen ligands using
[18F]-FES [46]. In a multicenter phase I trial, the
biologic effective dose (BED) of a novel ER-targeted
was determined using [18F]-FES [66]. They hypothesized that the coupling of optimal dose and maximum
pharmacologic effect could best assess ER
blockade through baseline and post-therapy imaging. In early-phase, clinical trials of novel
ER-targeting therapeutics, the use of [18F]-FES PET
has now become common to successfully determine the BED for multiple agents [67–69].
f
g
h
i
j
(arrows) and physiologic bone uptake in the thoracic spine
(dotted arrows). However, positive [
seen in the axillary lymph nodes (f–h; arrows) and the rst
thoracic vertebra (f, i, j; dotted arrows). (Adopted from
62])
[
18
F]-FES uptake is
cers, such as uterine cancers. It is well known that
18
the uptake of [
F]-FES and [18F]-FDG is especially useful for the differential diagnosis of endometrial hyperplasia in low-grade and high- grade
endometrial cancer. In particular, the characteristics of low-grade endometrial carcinomas are
decreased uptake of [18F]-FES, increased uptake
of [18F]-FDG, with an increased ratio of [18F]-FDG
to [18F]-FES uptake [70, 71]. On the opposite
high-grade carcinomas show an increased
[18F]-FDG to [18F]-FES uptake ratio. In the same
manner, malignant uterine sarcomas demonstrate
18
lower [
F]-FES uptake and a higher [18F]-FDG to
[18F]-FES uptake ratio allowing differentiation
between benign uterine leiomyomas and malignant uterine sarcomas [72, 73]. Additionally, other
studies show the use of [18F]-FES to imaging the
majority of ovarian cancers that express ER
[74–76].
16.4.6 Utilization of18F-FES inOther
Populations
As analogous to estradiol, [18F]-FES PET can use
as a PET radiotracer for other ER-expressing can-
16.5 Clinical Cases
Case 1 [77] (Fig.16.9)
Case 2 [78] (Fig.16.10)
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Fig. 16.9 A 73-year-old female underwent lymphatic
node ultrasonography, and core-needle biopsy showed
carcinoma invasive NST G1 (Ki67 1%), ER (3+) 100%,
and HER-2 negative in both breasts. PET/CT with 18FFES showed pathological uptakes in both breast tumors,
but lymph node packages in the left axilla and enlarged
cervical nodes were not estrogen-positive metastasis from
breast cancer. Therefore, a core-needle biopsy of the left
axilla lymph node was done with the result of DLBCL
Ki67 90%. For DLBCL staging, PET/CT with [
18
F]-FDG
was performed. The pathological uptakes were present in
the left axilla tumor and enlarged cervical nodes. In this
case, PET/CT with [
18
F]-FDG and [18F]-FES performed
along with FNA or core-needle biopsy allows for establishing the right diagnosis and the stage of both diseases.
Case 1 [77]
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M. R. Ruggiero et al.
Fig. 16.10 A 64-year-old female with multiple metastases from breast cancer showed the same degree of accumulation of [
lymphadenopathy, whereas higher 18F-FES uptake than
18
[
F]-FDG uptake was detected in right supraclavicular
lymphadenopathy. In patients with multiple metastases
from breast cancer, the combination of [
18
[
F]-FDG-PET imaging studies has the potential to reect
18
F]-FDG as [18F]-FES in left hilar
16.6 PET/CT Acquisition Protocol
Prior recommendations for [18F]-FES use can be
found in Venema etal. [79] and Kurland et al.
[80]. Thus prescribing information is available
from the FDA label [18]. Before administering
[18F]-FES, it is important to conrm the patient is
18
F]-FES and
tumor heterogeneity and characterize the in vivo tumor
phenotype. The index of the [
ratio could be used as a determinant of hormonal therapies
such as tamoxifen and aromatase inhibitor for breast cancer and pregestational agents and gonadotropin-releasing
hormone agonists for gynecological tumors. Case 2 [78]
18
F]-FDG: [18F]-FES SUV
not pregnant and not using selective estrogenic
receptor modulators, such as tamoxifen, or selective estrogenic degraders (SERDs), such as fulvestrant. Current guidelines suggest withdrawal
from tamoxifen for 8weeks and withdrawal from
fulvestrant for 28 weeks. The recommended
administered dose is 111–222MBq of FES (often
16 18F-FES
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185 MBq), administered over 1–2 min. PET
imaging is to begin 20–80 min (often 60min)
after radiopharmaceutical administration.
16.7 Variants andPitfalls
In the clinical practice, the main limitation of the
use of [18F]-FES is hard detection of liver metastases due to high hepatic uptake. Rapid blood
clearance, leading to lower tumoral uptake, and
low selectivity for ERα and ERβ, resulting in
reduced specicity of the procedure, are other
undeniable pitfalls of this radiotracer. For this
reason, additional estradiol analogs have been
developed. Most relevant for the clinical practice
may be radiopharmaceuticals such as 4-uoro11β -methoxy-16α -[18F]-fluoroestradiol
(4FM-[18F]F-FES) [81] and 1-(2-(2-(2-[18F]uoroethoxy)ethoxy)ethyl)-1H-1,2,3-triazoleestradiol ([18F]F-FETE) [82] to improve target
selectivity. As detector of functional ER,
[18F]-FES could not detect unfunctional ER, still
expressed in tumors. Thus, the lower sensitivity
for predicting the response to endocrine therapy
in breast cancer patients is strongly correlated
with [18F]-FES uptake and the degree of stromal
components [40]. Therapy like selective estrogen
receptor modulators or degraders (e.g., SERMs
or SERDs) must be discontinued before the PET
imaging to avoid interference with [18F]-FES
uptake [18].
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