Japanese Journal of Radiology
https://doi.org/10.1007/s11604-020-01040-1

ORIGINAL ARTICLE

Transarterial fiducial marker implantation for CyberKnife radiotherapy
to treat pancreatic cancer: an experience with 14 cases
Akira Imaizumi1 · Takuji Araki1 · Hiroki Okada1 · Yu Sasaki1 · Takafumi Komiyama1 · Toshihiro Suzuki2 ·Hiroshi Takahashi2 · Hiroshi Onishi1
Received: 31 March 2020 / Accepted: 26 August 2020
© The Author(s) 2020

Abstract
Purpose The purpose of this study was to evaluate the safety and feasibility of transarterial fiducial marker implantation for
CyberKnife radiotherapy to treat locally advanced pancreatic cancer.
Materials and methods Fifteen pancreatic cancer patients were enrolled for transarterial marker implantation. Embolization platinum coils were implanted as a fiducial marker within 20 mm of the cancer edge, and preferably within 3 mm. The
technical success of the implantation was defined as implantation of at least one fiducial marker within 20 mm of the target
tumor. Irradiation was performed using the CyberKnife system.
Results For 14 of 15 patients, transarterial implantation was successfully performed, and for 13 of 14 patients, the tracking
marker was implanted within 3 mm of the cancer. Tracking instability was observed in two patients, but irradiation was
accomplished in all 14 patients. No major complications caused by the implantation procedure were observed. The medianoverall survival after irradiation was 13.8 months, and the 1- and 2-years survival rates were 62.9% and 32.3%, respectively.
Conclusion Transarterial fiducial marker implantation for pancreatic cancer can be safely performed for tracking, and it will
be a valuable alternative approach to percutaneous fiducial marker implantation.
Keywords Transarterial fiducial marker implantation · Pancreatic cancer · CyberKnife radiotherapy · Real-time tumor
tracking

Introduction
Previous studies have shown that CyberKnife radiotherapy
is effective in patients with locally advanced pancreaticcancer [1]. This therapy decreases delays in the systemictreatment of pancreatic cancer while increasing local tumor
control. Local tumor control improves patient quality of life,
by controlling pain and decreasing the occurrence of gastricobstruction or duodenal obstruction [2]. Further, local control of tumors achieved through CyberKnife radiotherapy
prevents distant metastasis [2]. Real-time tumor tracking
during CyberKnife radiotherapy is currently used in thetreatment of lungs, abdominal, and pelvic tumors, whichhave respiratory movement. The pancreas is an organ that has
respiratory movement [3]. Therefore, to perform CyberKnife
radiotherapy for pancreatic cancer, real-time tumor tracking
is needed. For implantation of fiducial marker to real-timetracking, computed tomography (CT) or ultrasound (US)guided percutaneous implantation is commonly used [4, 5].
However, the percutaneous approach is difficult to perform
when other organs are located between the puncture point
and the target. To overcome this, we performed transarterial
fiducial marker implantation by microcatheter, guided byangiography. In this study, we evaluated the technical andclinical outcomes of transarterial marker implantation for
CyberKnife radiotherapy in pancreatic cancer.

* Akira Imaizumi
aimaizumi@yamanashi.ac.jp
1

Department of Radiology, Yamanashi University, 1110
Shimokato, Chuo, Yamanashi 409‑3898, Japan

2

Kasugai CyberKnife Rehabilitation Hospital, 436 Kokufu,
Kasugai‑cho, Fuefuki, Yamanashi 406‑0014, Japan

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Japanese Journal of Radiology

Materials and methods
Patients
Between September 2012 and December 2016, 17 patientswere diagnosed with pancreatic cancer and judged as unable to undergo surgical resection due to local progression,
distant metastasis, or advanced age. They were referredto our hospital for CyberKnife therapy. Fiducial marker
implantation was required to perform CyberKnife therapy
for real-time tumor tracking. Radiation oncologists andinterventional radiologists assessed each case by pre-procedural imaging studies (CT, magnetic resonance imaging(MRI) (Fig. 1a), and judged that in 15 of 17 patients, percutaneous marker implantation was too difficult to perform
due to a patient’s anatomical features and/or target lesion
location (another organ located between the tumor andpuncture sight, or the target was too far from the skin).
The characteristics of the 15 patients included in this study
are shown in Table 1. Eleven of 15 patients had a historyof systemic chemotherapy before and/or after Cyberknife
therapy. The other four patients had no history of chemotherapy during the progress. The institutional review

Fig. 1  An example case oftransarterial marker implantation for pancreatic tail cancer.
a Pre-procedural dynamic
contrast-enhanced (CE) CT
was performed to reveal thetumor location (marked bywhite arrow). b A microcatheter is inserted into the arterybranch near the target cancer
and angio-CT is performed todetermine the location of the
microcatheter tip (white arrow)relative to the target cancer.
Residual contrast media injectedin the previous angiography
also appears on this image. c, d
Post-procedural angiogram of
the implanted fiducial marker(black arrow; 2 pieces of 5-mmlong straight embolization
microcoils with a 0.018-inch
diameter)

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board of our hospital approved the study protocol, and all
patients gave written informed consent for the research
protocol and the procedure.

Fiducial marker implantation
All implantation procedures were performed using an angioCT unit (INFX 8000C/JU and Aquilion LB, CANON Medical Systems, Tochigi, Japan). Marker implantation was performed using the 3-Fr catheter system, which included a
3-Fr 25 cm sheath, a 3-Fr Shepard Hook type catheter, anda 2.0/2.4 Fr microcatheter (Carnerian Marvel, Tokai Medical
Products, Gifu, Japan). An embolization platinum microcoil
with a 0.018-inch diameter (Hilal®, Tornado® Embolization
Microcoil (Cook Medical, Indiana, USA)) was implanted asa fiducial marker. We chose the size and shape of coils by thetarget vessel size. If the target vessel was thin, the straightcoil seemed to be appropriate. On the other hand, when thetarget vessel was a little bit thick, we chose the single-curlor multi-curl coil, because curled coils had stronger radial
force than straight type and had lower risk of distal migration. First, digital subtraction angiography (DSA) was performed on the superior mesenteric artery (SMA) and theceliac artery (CA) to determine the arterial anatomy. Second,Japanese Journal of Radiology
Table 1  Patient characteristics (n = 15)

Table 2  Dose constraints

Characteristics

Value

LocationSex (male: female)Age (years)
Mean (range)
Local ­progressiona (T2:T3:T4:recurrence)
Tumor location in pancreas (head:body:tail)
Lymph node m­ etastasisa (N0:N1 and above)
Distal ­metastasisa (M0:M1)
History of chemotherapy (yes/no)
Chemotherapy before RT
GEM + S-1
S-1 only
GEM only
nab-PTX + GEM
Chemotherapy after RT
nab-PTX + GEM + nivolumab
nab-PTX + GEM
GEM only
S-1 only
RT dose (Gy)Median (range)
RT fraction
Median (range)

10:5

StomachDuodenum
Small intestine
Esophagus
Trachea/bronchus
Heart
Large vessel
Spinal cord

70.6 (41–88)
2:2:8:3
7:6:2
11:4
12:3
11:4c
7b
1
4
1
1
5b
1
1
1
2
50 (40–60)
10 (5–15)

RT radiotherapy, GEM gemcitabine, nab-PTX nab-paclitaxelab

UICC TNM Classification of Malignant Tumors, 8th edition
An overlap existed before and after RT

the artery branch nearest to the target tumor was identified
and the microcatheter was inserted into the artery branch.
Third, plain CT was performed to confirm that the tip ofthe microcatheter was located near the target lesion. If therelationship between catheter tip and target tumor was still
unclear on this plain CT, selective contrast-enhanced CT
was performed. Then, one or two pieces of embolizationcoil were implanted in parallel by position (Fig. 1b); they
formed one group of markers. The intended implantation
position was within 20 mm of the cancer edge, and preferably within 3 mm. One or two groups of markers were
implanted; in most cases, irradiation was available with only
one marker. However, in our earlier cases, another marker
was implanted as a backup. Post-procedural CT was performed to determine if the coil was correctly implanted near
the cancer edge, and if so, the implantation procedure wascompleted (Fig. 1c). All implantation procedures were performed within 2 or 3 days of hospitalization to watch theshort-time complications. If there was no bleeding at thepuncture site or other apparent symptoms after implantation and blood test results (blood count, C-reactive protein,serum amylase level) were within the normal range, thepatient was discharged and went to irradiation.

D1cc (Gy)

D10cc (Gy)

Dmax (Gy)< 144 Gy

< 105 Gy–

< 160 Gy

< 120 Gy–

< 175 Gy

< 140 Gy–––

< 75 Gy

D1cc dose delivered to 1% of the target volume, D10cc dose delivered to 10% of the target volume, Dmax maximum dose

Radiation therapy
For all patients, the Synchrony® Respiratory Tracking System (Accuray, Sunnyvale, California, USA) was used forreal-time tracking the tumors. To create treatment plans, afour-dimensional treatment planning system (Multiplan version 5.2; Accuray, Sunnyvale, California, USA) was used,
and the CyberKnife G4 radiosurgery system (Accuray, Sunnyvale, California, USA) was used for treatment. Patientswere simulated in a supine position and immobilized witha vacuum cushion. Contrast-enhanced dynamic CT images
were used to identify the gross tumor volume (GTV). The
clinical target volume (CTV) was equal to the GTV. Internal
target volume (ITV) was obtained as the fiducial fusion of
CTV in inspiratory and expiratory phases. Safety margins
around the tumor of 3 mm in the lateral and vertical directions and 3.75 mm in cranio-caudal direction were added
to the ITV, and this was defined as planning target volume(PTV). Dose constraints for stereotactic body radiation
therapy for pancreatic cancer in our institution are listed
in Table 2. The α/β ratio of the biological equivalent dosewas 3 Gy. A total median dose of 50 Gy (range 40–60 Gy)
was delivered in 10 fractions (median, range 5–15) to the
PTV D95%. During treatment, respiratory tumor motion
was actively compensated for by the dynamic Synchrony®
Respiratory Tracking System.

Follow‑up assessment
Technical success of implantation was defined as implantation of at least one fiducial marker within 20 mm of thetarget tumor. Other recorded features used to assess success included the target artery, coil character, number of
implanted coils, distance from coil to target, total marker
length (measured using the MPR image of the post-procedural plain CT), number of markers, procedure duration, number of plain/contrast-enhanced CTs during theprocedure, availability of feather stable tracking (yes/no),13

Japanese Journal of Radiology

accomplishment of radiotherapy (RT) (yes/no), complications caused by the marker implantation procedure, and toxicity by RT (graded according to the NCI Common Terminology Criteria for Adverse Events, version 4.03). The total
marker length was defined as the maximum diameter of eachmarker group (Fig. 1d). Complication caused by the implantation was defined as any abdominal symptoms observed
after implantation or any vessel injury that occurred during
the angiography procedure. We asked patients to describe
their symptoms during hospitalization, and radiation oncologists performed follow-up interviews when the outpatient
visited for RT planning.

Statistical analysis
Overall survival (OS) and local progression-free survival
were determined after RT by generating survival curves
by the Kaplan–Meier method. The median survival monthand overall survival rate for 1 and 2 years were calculated
from the Kaplan–Meier plots. All statistical analyses were
performed with EZR (Saitama Medical Center, Jichi Medical University, Saitama, Japan), which is a graphical userinterface for R (The R Foundation for Statistical Computing,
Vienna, Austria). More precisely, it is a modified version
of R commander, designed to add statistical functions frequently used in biostatistics [6].

Results
Implantation and irradiation of each patient is diagrammedin Fig. 2 and summarized as follows. In 14 of 15 patients,
transarterial fiducial marker implantation was successfully
performed (a technical success rate of 93%). In 13 of 14
cases, the puncture site was the right femoral artery; in theone other patient, a left brachial approach was chosen since
he had a history of aortic artery repair. Transcatheter implantation of fiducial markers failed for only 1 of 15 cases. This
failure occurred because there was no appropriate artery
located near the pancreatic cancer target. In this case, we
performed CT again during the angiography procedure,
which indicated that CT-guided percutaneous implantation
was an available alternative, which we used for successful
implantation.
Selective contrast-enhanced CT was performed during
the procedure in four cases; in the other 10 cases, marker
implantation was accomplished with DSA and plain
CT only. For 13 of 14 patients, the tracking marker was
implanted within 3 mm of the cancer. Stable marker tracking was successful in 12 of 14 patients, as defined as theability of the CyberKnife to distinguish the fiducial markers.
In one case, each marker was implanted successfully but waslined up along a tracking fluoroscopy beam (Fig. 3). This
meant that the CyberKnife could not distinctly recognize

Fig. 2  Kaplan–Meier estimates of overall survival and local progression-free survival after radiation therapy of all patients (n = 14)

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Japanese Journal of Radiology
Fig. 3  Summary of patientfiducial marker implantationand irradiation

them as separate markers. Changing the patient’s position tothe oblique supine position and adjusting the RT setup enabled the tracking system to work correctly. In a second casewhere implantation occurred successfully, two 10-mm-longstraight coils were implanted around the pancreatic headcancer target (Fig. 4). Since a total marker length greaterthan 10 mm was too long for stable marker tracking, irradiation took longer but was completed without additional
marker implantation. Migration of the fiducial markers was
not observed in the 14 cases.
Ultimately, in all 14 cases in which the marker was
implanted by the transarterial procedure, irradiation was
accomplished. Complications caused by the implantation
procedure were not observed in any patient. Toxicity caused
by RT was observed in two cases; one was a grade 3 gastrichemorrhage and the second was a grade 2 duodenal ulcer. In
both cases, the target tumor location was the pancreas head.
The grade 2 patient was treated with medication. The grade
3 patient underwent endoscopic hemostasis, which failed,
and then trans-arterial embolization. The summary of all 15

Fig. 4  A case of tracking in parallel to the fluoroscopy beam. a Preprocedural dynamic contrast-enhanced (CE) CT of the cancer target
in the pancreas tail (white arrow). b Post-procedural plain CT showscases is presented in Table 3. The median follow-up period
after the day of the beginning of RT was 368 days (range
84–964 days). The median overall survival after RT was
13.8 months (95% confidence interval (CI): 4.67–N/A). The
1-year and 2-year overall survival rates were 62.9% (95%CI = 0.323–0.826) and 32.3% (95% CI = 0.085–0.596),
respectively (Fig. 5). The median time to local progression was 10.7 months (95% CI = 5.4–N/A). The 1-year and2-year local progression-free survival rates were 50.0% (95%CI = 0.229–0.722) and 26.8% (0.073–0.515), respectively.

Discussion
Here, transarterial fiducial marker implantation for
CyberKnife radiotherapy was successful in fourteen cases
to treat locally advanced pancreatic cancer, demonstratingthat this technique is an effective alternative to the percutaneous approach. In the case where tracking was unable tooccur, the target cancer was located on the pancreas tail andtwo fiducial markers that were implanted on opposite ends of the cancer aligned with a fluoroscopy beam (white arrow), preventing the
CyberKnife system from distinguishing the two separate markers

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Japanese Journal of Radiology
Fig. 5  A case of unstable tracking. a Pre-procedural dynamic
contrast-enhanced (CE) CT ofthe cancer target in the pancreas
head (black arrow head). b Twostraight-shaped coils 10 mm inlength were implanted nearby
the cancer. c The post-implantation fluoroscopy image showsthat the total marker length was
too long for stable tracking

the two markers were implanted on opposite ends, in parallel to the fluoroscopy beam, which prevented recognition
by CyberKnife tracking. Tracking was enabled only after
adjusting the patient’s position during RT setup. The incident angle of the CyberKnife tracking system’s fluoroscopy
beam is about 45° to the horizontal line; from this case, it
is clear that the markers should not be implanted parallel tothis 45° line.

13

In the case of unstable tracking, fiducial marker tracking
by the CyberKnife system would sometimes stop. In thiscase, 2 pieces of 10-mm-long straight coils were implanted
in series in the same vessel, and the maximum length of the
combined markers was over 10 mm. In another case without tracking errors that we had experienced, the total lengthof the tracking marker was shorter than 8 mm. From that
instance, we considered that too-long marker lengths lead to

Head
Body
Body
Body
Head
Tail
Head
Head
Head
Body
Tail
Head
Body
Body
Head

1
2
3
4
5
6
7
8
9
10
11
12
13
14
15

No. ofmarkergroup

Coil ­charactera

ASPD, DPA
1
2-2HILAL
Convert to percutaneous implantation
LGA, MCA
2
C3 mm + 5 mm, 2-2HILAL
DPA, LGA
2
2-2HILALx2,7 mm
PSPD, MCA
2
2-2HILAL, 2-2HILAL
PMA, SpA
2
5 mm, 2-2HILALPSPD, ASPD
2
2-2HILAL, C3 mm
IPD, PSPD
2
5 mm × 2 5 mm × 3
PSPD
1
2-2HILAL
DPA, LGA
2
2–4, 2–4
DPA
1
C3 mm
IPD
1
10 mm × 2
DPA
1
C3 mm, 2-2HILAL
DPA
1
5 mm × 2
DPA
1
2-2HILAL

Target artery< 3 mm< 3 mm, 14 mm< 3 mm, 13 mm< 3 mm
7 mm, 9 mm
< 3 mm, 10 mm< 3 mm< 3 mm< 3 mm< 3 mm< 3 mm< 3 mm< 3 mm< 3 mmOk
Ok
Ok
Unable
Ok
Ok
Ok
Ok
Ok
Unstable
Ok
Ok
Ok

Distance to tumor

Ok

Stable tracking

6 mm/7 mm
5 mm/8 mm
5 mm/5 mm
7 mm/7 mm
4 mm/6 mm
6 mm/7 mm
5 mm
7 mm/8 mm
7 mm
13 mm
6 mm
6 mm
5 mm

4 mm

Total marker length

216
72
140
228
113
114
118
63
78
106
67
139
45

89

Procedure
duration(minute)

3
2
3
3
3
3
3
2
1
1
1
1
1

0

Number of
Plain CT

0
1
1
2
0
0
0
0
0
0
0
0
0

3

Number of
Selective
CE-CT

DPA dorsal pancreatic artery, ASPD anterior superior pancreaticoduodenal artery, PSPD posterior superior pancreaticoduodenal artery, IPD inferior pancreaticoduodenal artery, SpA
splenic artery, PMA pancreatic magna artery, MCA medial colic artery, LGA left gastric artery, 2-2HILAL 2 mm/2 mm-diameter helical-shaped coil, C3mm 3 mm-diameter C-shaped coil,
5 mm/7 mm/10 mm straight coil, 2–4 2 mm/4 mm-diameter tornado-shaped coil

Location

Patient

Table 3  Patient features

Japanese Journal of Radiology

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Japanese Journal of Radiology

unstable tracking. Before this case, we had considered that
too-small and short fiducial markers might have insufficientvisibility for stable tracking because of prior experience withunstable tracking using a single 5-mm coil (unpublished).
We had thought that the total size of the marker should belarger and longer. A phantom simulation experiment of ourinstitution suggested that the marker tracking might become
unstable when the maximum length of the markers was over
8 mm. These factors lead to our consideration that a coil thatwas too small and short might have insufficient visibility forstable tracking; however, a marker that is too long and large
is also problematic. Total marker length should be shorter
than 8 mm in future procedures, to ensure that stable tracking occurs.
Especially, in later cases, we performed the marker
implantation without CT angiography. In these cases, we
could find the adjacent vessel to the marker implantation
using DSA and plain CT only. It was up to the operator ineach case to decide whether to use CT angiography or not.
However, in some cases, we took too much time to accomplish the implantation. According to the retrospective review
of each procedure, much of the entire procedure time wasspent searching for the adjacent vessel. Although CT angiography requires considerable contrast agents and a bit of time,
it might provide information about the local anatomy andmight reduce the total procedure time. There could be room
for improvement regarding our method. Although not available in our institution, 3D vessel tracking software might behelpful to search for the adjacent vessel.
Before performing this transarterial implantation, we
expected that complications due to implantation were local
ischemic reactions caused by the embolizing function of
the implanted coil, but no complications caused by the
implantation procedure were observed. We reason that thetwo small pieces of coil have limited embolization power,
and pancreatic tissue has a rich arterial network and collateral pathway [7], so the local ischemic reaction was likely
limited and thus caused no clinical symptoms. Although it
was reported that the risk of severe complications caused
by a percutaneous approach is not very high, local hemorrhage and fiducial marker migration might occur [4].
One beneficial feature of transarterial implantation is thatthe needle used to insert the marker does not penetrate
the tissue between the puncture site and the target organ.
This potentially causes less injury to other organs in thepenetration tract and may reduce the risk of tumor dissemination and marker migration. In addition to CT or USguided percutaneous approaches, endoscopic ultrasound(EUS)-guided trans-gastrointestinal marker implantation
has been reported [8–10] as a successful technique. Thisis also good alternative technique, but there is not dedicated product for EUS-guided marker implantation, andit also requires the off-label fiducial marker use. Another13

characteristic of EUS-guided approach is that the marker
implantation might be more difficult when the target
locates on pancreatic tail. Based on the success of theseproceeds, as well as the transarterial approach detailed
here, we assert that the most appropriate implantation
procedure should be chosen based on patient background,target location, anatomical features, and the skills available at each institution.
According to previous reports, the median OS of pancreatic cancer treated by Cyberknife ranges from 10.6 to
18.6 months, 1-year OS ranges from 39.1 to 56%, andPFS ranges from 7.3 to 9.8 months [11–16]. Our reported
median OS and 1-year OS results were within the rangeof previous reports and PFS was a little bit higher. The
RT dose of our study (45–60 Gy/5–15 Fr) tended to behigher than other reports, which could explain the clinicaloutcome, limiting the conclusions that can be drawn fromthis study on the success of this approach. Further, thisstudy was limited by its nonrandomized patient inclusion,
because it was a single institution retrospective study.
In conclusion, we performed transarterial fiducial
marker implantation for real-time tracking of radiotherapy
in 14 pancreatic cancer patients without complication, andthis approach may be an alternative method for fiducial
marker implantation for real-time tracking of irradiation
when other approaches are difficult to perform.
Acknowledgements The authors would like to thank Editage (www.
edita​ge.jp) for English language editing.
Funding This research received no specific grant from any funding
agency in the public, commercial, or not-for-profit sectors.

Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict ofinterest.
Ethical approval All procedures performed in these studies involving
human participants were in accordance with the ethical standards ofthe institutional and/or national research committee and with the 1964
Helsinki Declaration and its later amendments. The institutional review
board of our hospital approved the study protocol, and all patients gave
written informed consent for the research protocol and the procedure.
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as longas you give appropriate credit to the original author(s) and the source,
provide a link to the Creative Commons licence, and indicate if changes
were made. The images or other third party material in this article areincluded in the article’s Creative Commons licence, unless indicatedotherwise in a credit line to the material. If material is not included in
the article’s Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you willneed to obtain permission directly from the copyright holder. To view acopy of this licence, visit http://creat​iveco​mmons​.org/licen​ses/by/4.0/.

Japanese Journal of Radiology

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