Respiratory Motion Artefacts in Primovist

PLOS ONE
RESEARCH ARTICLE
Respiratory motion artefacts in Gd-EOB-DTPA

(Primovist/Eovist) and Gd-DOTA (Dotarem)-
enhanced dynamic phase liver MRI after
intensified and standard pre-scan patient
preparation: A bi-institutional analysis
Christian Wybranski1‡, Florian Siedek ID1‡*, Robert Damm2, Angelos Gazis2,
Ortrud Wenzel2, Stefan Haneder1, Thorsten Persigehl1, Susanne Steinhauser3,
a1111111111
Maciej Pech ID2, Frank Fischbach2, Katharina Fischbach2
a1111111111
a1111111111 1 Institute of Diagnostic and Interventional Radiology, Faculty of Medicine and University Hospital of
a1111111111 Cologne, University of Cologne, Cologne, Germany, 2 Department of Radiology and Nuclear Medicine,
a1111111111 University Hospital of Magdeburg, Magdeburg, Germany, 3 Institute of Medical Statistics and Computational
Biology, University Hospital of Cologne, Cologne, Germany
‡ CW and FS are Joint First Authors to this work.

* [email protected]
OPEN ACCESS
Citation: Wybranski C, Siedek F, Damm R, Gazis A, Abstract

Wenzel O, Haneder S, et al. (2020) Respiratory
motion artefacts in Gd-EOB-DTPA (Primovist/
Eovist) and Gd-DOTA (Dotarem)-enhanced
dynamic phase liver MRI after intensified and Objective
standard pre-scan patient preparation: A bi- The objective of this study is to evaluate if intensified pre-scan patient preparation (IPPP)
institutional analysis. PLoS ONE 15(3): e0230024.
that comprises custom-made educational material on dynamic phase imaging and super-
https://doi.org/10.1371/journal.pone.0230024
vised pre-imaging breath-hold training in addition to standard informative conversation with
Editor: Pascal A. T. Baltzer, Medical University of
verbal explanation of breath-hold commands (standard pre-scan patient preparation–
Vienna, AUSTRIA
SPPP) might reduce the incidence of gadoxetate disodium (Gd-EOB-DTPA)-related tran-
Received: November 25, 2019
sient severe respiratory motion (TSM) and severity of respiratory motion (RM) during
Accepted: February 18, 2020 dynamic phase liver MRI.
Published: March 20, 2020
Copyright: © 2020 Wybranski et al. This is an open Material and methods

access article distributed under the terms of the
In this bi-institutional study 100 and 110 patients who received Gd-EOB-DTPA for dynamic
Creative Commons Attribution License, which
permits unrestricted use, distribution, and phase liver MRI were allocated to either IPPP or SPPP at site A and B. The control group
reproduction in any medium, provided the original comprised 202 patients who received gadoterate meglumine (Gd-DOTA) of which each 101
author and source are credited. patients were allocated to IPPP or SPPP at site B. RM artefacts were scored retrospectively
Data Availability Statement: All relevant data are in dynamic phase images (1: none– 5: extensive) by five and two blinded readers at site A
included in the Supporting Information files. The and B, respectively, and in the hepatobiliary phase of the Gd-EOB-DTPA-enhanced scans
actual raw imaging data from our patients are
by two blinded readers at either site.
completely restricted due to legal and ethical
restrictions on sharing these data because of
potentially identifying or sensitive patient Results
information, imposed by federal law and the ethics
committee of the University clinic of Cologne and The incidence of TSM was 15% at site A and 22.7% at site B (p = 0.157). IPPP did not
Magdeburg reduce the incidence of TSM in comparison to SPPP: 16.7% vs. 21.6% (p = 0.366). This
PLOS ONE | https://doi.org/10.1371/journal.pone.0230024 March 20, 2020 1 / 16

PLOS ONE Respiratory motion in dynamic phase liver MRI after intensified and standard pre-scan preparation
Funding: The authors received no specific funding finding was consistent at site A: 12% vs. 18% (p = 0.401) and site B: 20.6% vs. 25% (p =
for this work. 0.590). The TSM incidence in patients with IPPP and SPPP did not differ significantly
Competing interests: I have read the journal’s between both sites (p = 0.227; p = 0.390). IPPP did not significantly mitigate RM in compari-
policy and the authors of this manuscript have the son to SPPP in any of the Gd-EOB-DTPA-enhanced dynamic phases and the hepatobiliary
following competing interests: Katharina Fischbach
and Frank Fischbach received consultant fees from
phase in patients without TSM (all p�0.072). In the Gd-DOTA control group on the other
Bayer Healthcare. This does not alter our hand, IPPP significantly mitigated RM in all dynamic phases in comparison to SPPP (all
adherence to PLOS ONE policies on sharing data p�0.031).
and materials All other authors have declared that
no competing interests exist.
Conclusions
We conclude that Gd-EOB-DTPA-related TSM cannot be mitigated by education and train-
ing and that Gd-EOB-DTPA-related breath-hold difficulty does not only affect the subgroup
of patients with TSM or exclusively the arterial phase as previously proposed.
Introduction
Respiratory motion (RM) during liver dynamic phase contrast-enhanced Magnetic Resonance
Imaging (DCE-MRI) substantially degrades image quality and increases the economic burden
for health care systems if examinations need to be repeated. Transient severe respiratory
motion (TSM) is a well-known phenomenon after administration of gadoxetate disodium
(Gd-EOB-DTPA; Primovist1/Eovist1, Bayer HealthCare Pharmaceuticals) that might
impede image interpretation especially of the hepatic arterial phase. The reported incidence of
TSM shows a considerable variation of 5–22% between institutions [1–8]. Its pathophysiology
is not yet fully understood.
A technical approach to mitigate the effects of Gd-EOB-DTPA-related TSM comprises accel-
erated MR imaging with short breath-hold times [9–11], multiple arterial phase imaging [12] or
free breathing protocols [13,14]. However, these imaging techniques require sophisticated
hard- and software, which might not be available at every institution and despite these techno-
logical advances, best image quality is achieved in patients without RM during dynamic phase
image acquisition. Alternative strategies to reduce the incidence of TSM and severity of RM in
the first place are urgently needed. One alternative strategy that has been described previously
to minimize TSM was the modification of the injection protocol of Gd-EOB-DTPA. Kim et al.
[15] as well as Polanec et al. [16] found a 50% dilution of Gd-EOB-DTPA at an injection rate of
2mL/s [15] or 1mL/s [16] while Davenport et al. [17] found a fixed dose of 10mL instead of
20mL to reduce Gd-EOB-DTPA-related TSM significantly. Another alternative strategy
recently described was a modified breathing command that has been advocated to reduce Gd-
EOB-DTPA-related TSM [18,19]. The rationale behind this modification was that accustoming
patients to the pace and nature of breath-holding would be beneficial to reduce RM in general
and consequently also TSM. Another important aspect with regards to Gd-EOB-DTPA-related
TSM that has not been evaluated in detail yet is pre-scan patient preparation. Explanation of
dynamic phase imaging and breathing commands during informative conversation before
image acquisition is clinical standard of care (standard pre-scan patient preparation–SPPP), yet
communication about the significance of dynamic phase imaging for diagnosis and the effects
of RM might differ between institutions. To the best of our knowledge, supervised pre-imaging
breath-hold training is not routinely performed in all institutions. These factors might contrib-
ute to the variable incidence of Gd-EOB-DTPA-related TSM.
Hence, the purpose of our bi-institutional study was to investigate if intensified pre-scan
patient preparation (IPPP) that focusses on dynamic phase imaging and comprises custom-

made educational material and standardized breath-hold training might reduce the incidence
of Gd-EOB-DTPA-related TSM and the severity of RM during liver DCE-MRI. The effect of
IPPP was crosschecked in patients who received gadoterate meglumine (Gd-DOTA;
Dotarem1, Guerbet) for dynamic phase imaging.
Materials and methods

The ethical commission of the Otto-von-Guericke University and the University Clinic of
Magdeburg, Germany, (Approval number: 31/14) and the ethical commission of the Univer-
sity of Cologne, Germany, (Approval number: 18–225) both waived the need for consent as all
studies were necessary and medically indicated and our intervention did not influence patient
care or patient health while all patient data were also analyzed anonymously. Hereafter, the
University Clinic of Magdeburg, Germany, is referred to as site A while the University Clinic
of Cologne, Germany, is referred to as site B.
Standard pre-scan preparation (SPPP)

SPPP was performed consistently at both sites and comprised informative conversation
accompanied by standardized informed consent documentation (Thieme Compliance1). All
patients were informed about the necessity of breath-holding during dynamic phase imaging,
potential sensations associated with contrast agent administration and how to behave at the
onset of dyspnea.
Intensified pre-scan preparation (IPPP)

IPPP comprised all preparatory steps taken in SPPP. During informative conversation an addi-
tional focus was placed on dynamic phase image acquisition, such as the number of acquired
phases and diagnostic importance of each phase. Custom-made educational material illus-
trated the effects of RM during image acquisition (Fig 1). Supervised breath-hold training
comprised two 20 s breath-hold cycles measured by means of a stopwatch, which were initi-
ated with the same breath-hold command employed during dynamic phase imaging and
patients were instructed to continue shallow and regular breathing at the onset of moderate
but still bearable dyspnea.
Patient allocation to SPPP and IPPP

At site A, one board certified radiologist performed IPPP in 50 consecutive patients scheduled
for Gd-EOB-DTPA-enhanced liver MRI in between May–August 2013 without dedicated ran-
domization based on the radiologist’s duty in the MRI unit. Fifty consecutive patients with
SPPP within the study interval constituted the control group.
At site B, IPPP and documentation of the accomplished breath-hold duration was per-
formed consecutively in 58 and 101 patients scheduled for Gd-EOB-DTPA- and Gd-DOTA-
enhanced dynamic phase imaging by several specialized MR-technicians in between October
2016 –February 2018 without dedicated randomization based on the technicians’ duty in the
MRI unit. The technicians who performed IPPP were not involved in the final image acquisi-
tion. Fifty-two and 101 consecutive patients scheduled for Gd-EOB-DTPA- and Gd-DOTA-
enhanced dynamic phase imaging received SPPP within the study period. The assignment of
patients into either group was neither influenced by the investigators nor referring physicians.
Patient allocation at both sites is depicted in Fig 2.

Fig 1. Educational material for intensified pre-scan preparation (IPPP). Educational material employed to illustrate
the effects of breathing motion during dynamic phase imaging as part of intensified pre-scan preparation (language
has been translated for publication purpose).
https://doi.org/10.1371/journal.pone.0230024.g001
Image acquisition
The detailed technical parameters of T1-weighted (T1w) pre-contrast, dynamic phase imaging
and hepatobiliary phase at site A and B are presented in Table 1.
Site A employed exclusively Gd-EOB-DTPA (0.25 mmol/mL) for liver imaging at a fixed
dose of 10 milliliters (mL) administered intravenously with an injection rate of 1 mL/s using
an automated power injector (Accutron1, Medtronic), followed by a 30 mL saline chaser at
the same injection rate. Bolus tracking was used to detect contrast agent arrival in the distal
thoracic aorta.
Site B employed Gd-EOB-DTPA (0.25 mmol/mL) or Gd-DOTA (0.5 mmol/mL) for liver
imaging based on site specific standard operating procedures (SOPs) and/or the request of the

Fig 2. Study flow chart. Patient allocation as well as image analysis protocol for both sites is illustrated. � = HBP:
hepatobiliary phase (only applicable in Gd-EOB-DTPA-enhanced scans).
referring physicians. Gd-EOB-DTPA was administered intravenously at a fixed dose of 10 mL

with an injection rate of 2 mL/s by means of an automated power injector (Spectris Solaris
EP1, Medrad, Bayer Healthcare), followed by a 30 mL saline chaser injected at the same rate.
Gd-DOTA was administered weight-adapted with a dose of 0.2 mL/kg with the same injection
parameters. Bolus tracking was performed to detect contrast agent arrival in the distal thoracic
aorta. Both sites employed an automated breathing command during dynamic phase imaging

Table 1. Technical MRI parameters at sites A and B.
Site A Site B
Imaging System Intera Ingenia Ingenia
(Philips Healthcare) (Philips Healthcare) (Philips Healthcare)
Main magnetic field strength 1.5 T 1.5 T 3.0 T
Receiver coil Torso 16-channel Torso 32-channel Torso 32-channel
Image sequence T1 FFE 3D T1 FFE 3D T1 FFE 3D
Repetition/Echo time (TR/TE; ms) 3.9/1.84 5.2/2.6 shortest/shortest
Reconstructed voxel (mm) 1.0 x 1.0 x 3.0 0.69 x 0.69 x 3.0 1.04 x 1.04 x 2.5
Sense factor (anterior-posterior/feet-head) 1.8/1.0 2.0/1.2 2.3/1.3
Acquisition time for dynamic phases (s) 14.6 17.0 13.0
Bolus track distal thoracic aorta distal thoracic aorta distal thoracic aorta
Delayed arterial phase (s) 20 20 20
Portal venous phase (s) 60 60 60
Late venous phase (s) 180 240 240
Hepatobiliary phase (min)� 20 20 20
Imaging parameters were consistent in pre-contrast and dynamic image phases after contrast agent administration. T = Tesla; FFE = Fast field echo; � = only applicable
after Gd-EOB-DTPA administration.
https://doi.org/10.1371/journal.pone.0230024.t001
generated by the imaging system (auto voice): patients were instructed to breathe in and out
and stop breathing for image acquisition.
Image analysis
The pre-contrast, arterial, portal venous, transitional and hepatobiliary phase (HBP: only
applicable in Gd-EOB-DTPA-enhanced scans) images were anonymized, randomized and
loaded separately onto the PACS systems. Five blinded board certified radiologists (HBP: two
Fig 3. Image examples for TSM after Gd-EOB-DTPA administration. Images (a)-(d): 41-year-old female patient with breast
carcinoma and hepatic metastases with TSM after Gd-EOB-DTPA administration. RM scores: 1.0 –pre-contrast; 3.5 –arterial phase; 2.0
–portal venous phase; 1.0 transitional phase. The patient received IPPP prior to imaging. Images (e)-(h): 59-year-old female patient with
neuroendocrine pancreatic cancer with TSM after Gd-EOB-DTPA administration RM scores: 1.0 –pre-contrast; 5.0 –arterial phase; 1.0
–portal venous phase; 1.0 transitional phase. The patient did receive SPPP prior to imaging. TSM = Transient severe respiratory motion.

blinded board certified radiologists) at site A and two blinded board certified radiologists at
site B independently analyzed the images for severity of RM. RM was graded according to Dav-
enport et al. [1,2]: Grade 1 = none, Grade 2 = minimal, Grade 3 = moderate with some
impairment of image quality, Grade 4 = severe with substantial impairment of image quality,
Grade 5 = uninterpretable images (see Fig 3). TSM was diagnosed, if the RM grade differed
by � 2 points between pre-contrast and arterial phase image with return to pre-contrast values
in portal venous or transitional phase (Fig 3). Patients with RM grade of � 3 in pre-contrast
phase were not assigned to the TSM group. The hepatobiliary phase after Gd-EOB-DTPA
administration, though not part of the dynamic contrast phases per se, was partly included in
the analysis as it might allow a sufficient detection and characterization of focal liver lesions,
especially when the arterial phase is uninterpretable due to severe TSM. Accordingly, in addi-
tion to the dynamic phases it is also important that the hepatobiliary phase is artifact-free or
only has minor artifacts.
Evaluation of risk factors for Gd-EOB-DTPA-related TSM

Patient characteristics including comorbidities and potential risk factors for TSM were
retrieved from the electronic medical record system. Pleural effusion and ascites were mea-
sured in the MR images and were scored as moderate (<2 and <5 cm) or severe (>2 and >5
cm). Signs of lung fibrosis or emphysema were evaluated as present or absent in computed
tomography studies, whenever available.
Statistical analysis
Statistical analyses were performed using SPSS Statistics for Windows, version 23.0 (IBM
Corp., Armonk, NY). Continuous variables are presented as the median and interquartile
range (25th - 75th percentile) and categorical variables as numbers and percentages. RM scores
are additionally presented as the mean ± SD. Inter-reader agreement was assessed by calculat-
ing the absolute agreement, single measure intra-class correlation coefficient (ICC), applying a
two-way random effect model. Pairwise comparisons were performed using the Mann-Whit-
ney U test for continuous variables and Pearson’s χ2 test or Fisher’s exact test for categorical
variables. Fisher’s exact test was performed if at least one cell had an expected count < 5. All
reported p-values were calculated based on two-sided test hypotheses and p-values of �0.05
were considered statistically significant. As the analyses were regarded as explorative, we did
not adjust for multiple testing.
Results
Inter-reader agreement for grading of respiratory motion artefacts
The inter-reader agreement for RM grading was excellent (>0.8) or very good (>0.7) at site A
and B with ICCs of 0.86 and 0.77 (pre-contrast), 0.92 and 0.89 (arterial), 0.87 and 0.87 (portal
venous), 0.84 and 0.73 (transitional phase) as well as 0.86 and 0.75 (hepatobiliary),
respectively.
IPPP and SPPP in Gd-EOB-DTPA-enhanced dynamic phase imaging

Patients allocated to SPPP and IPPP did not differ significantly in any of the baseline charac-
teristics (all p�0.129; Table 2). TSM was observed in 15/100 patients at site A (15.0%) and 25/
110 patients at site B (22.7%, p = 0.157). IPPP did not significantly reduce the incidence of
TSM in comparison to SPPP: 18/108 patients with IPPP (16.7%) vs. 22/102 patients with SPPP
(21.6%; p = 0.366). This finding was consistent at site A: 6/50 patients with IPPP (12%) vs. 9/50

Table 2. Characteristics of patients allocated to either SPPP or IPPP in the Gd-EOB-DTPA and Gd-DOTA group.
Pre-scan preparation: Gd-EOB-DTPA Pre-scan preparation: Gd-DOTA Gd- Gd-DOTA

EOB-DTPA
standard intensified p= standard intensified p= all patients all patients p=
Number of 102 108 101 101 210 202
patients
Gender female 48 (47.1) 59 (54.6) 0.273 41 (40.6) 29 (28.7) 0.052 107 (51) 70 (34.7) 0.001
male 54 (52.9) 49 (45.4) 60 (59.4) 72 (71.3) 103 (49) 132 (65.3)
Age (years) median (IQR) 63.4 (52.6– 60.9 (53.6– 0.538 60.7 (52.5– 65.0 (53.9– 0.225 61.7 (53.4– 62.8 (53.6– 0.851
74.0) 71.5) 70.5) 71.5) 73.4) 70.9)
BMI (kg/m2) �� median (IQR) 25.5 (22.2– 24.7 (22.5– 0.929 26.8 (24.7– 26.7 (24.6– 0.898 24.8 (22.4– 26.7 (24.6– 0.013
31.2) 29.9) 31.1) 31.5) 30.1) 31.4)
Tumor etiology HCC/CCC 17 (16.7) 22 (20.4) 0.700 25 (24.8) 22 (21.1) 0.923 39 (18.6.3) 48 (23.8) <0.001
metastasis 48 (47.1) 52 (48.1) 15 (14.9) 15 (14.9) 100 (47.6) 29 (14.4)
no 37 (36.2) 34 (31.5) 61 (60.3) 64 (63.3) 71 (33.8) 125 (61.9)
malignancy
Acquisition time 13.0 34 (33.3) 40 (37.0) 0.854 63 (62.4) 68 (67.3) 0.461 74 (35.2) 131 (64.9) <0.001
(s)
14.6 50 (49.0) 50 (46.3) . . 100 (47.6) 0 (0.0)
17.0 18 (17.6) 18 (16.7) 38 (37.6) 33 (32.7) 36 (17.1) 71 (35.1)
Prior MRI yes 56 (54.9) 63 (58.3) 0.616 64 (63.3) 63 (62.3) 0.884 119 (56.7) 127 (62.9) 0.199
median (IQR) 2 (1–4) 2 (1–5) 0.233 2 (1–5) 2 (1–4) 0.451 2 (1–5) 2 (1–5) 0.663
Prior TSM yes 16 (15.7) 26 (24.1) 0.129 . . 42 (20) .
Pleural effusion yes 11 (10.8) 6 (5.6) 0.165 13 (12.9) 9 (8.9) 0.249 17 (8.1) 22 (10.9) 0.333
< 2cm 9 (8.8) 5 (4.6) >0.999 10 (9.9) 7 (6.9) >0.999 14 (6.6) 17(8.4) 0.824
> 2cm 2 (2.0) 1 (0.9) 3 (3.0) 2 (2.0) 3 (1.5) 5 (2.5)
Ascites yes 9 (8.8) 8 (7.4) 0.707 18 (17.8) 9 (8.9) 0.048 17 (8.1) 27 (13.4) 0.083
< 5cm 7 (6.8) 6 (5.5) >0.999 16 (15.8) 7 (6.9) 0.250 13 (6.2) 23 (11.4) 0.585
> 5cm 2 (2.0) 2 (1.9) 2 (2.0) 2 (2.0) 4 (1.9) 4 (2.0)
Cirrhosis yes 14 (13.7) 19 (17.6) 0.442 48 (47.5) 49 (48.5) 0.500 33 (15.7) 97 (48.0) <0.001
Lung fibrosis yes 3 (3.0) 6 (5.6) 0.366 3 (3) 2 (2) 0.500 9 (4.2) 5 (2.5) 0.293
CT CM allergy yes 4 (9.5) 2 (4.2) 0.412 1 (1.2) 3 (3.4) 0.621 6 (2.8) 4 (2.3) 0.097
Allergy general �� yes 10/52 (19.2) 12/58 (20.6) >0.999 23 (22.7) 28 (27.7) 0.859 22/110 (20.0) 51 (25.2) 0.476
Cardiac problems none 7/52 (13.4) 13/58 (22.4) 0.502 22 (21.8) 33 (32.6) 0.056 20/110 (18.2) 55 (26.2) 0.117
��
Categories are presented as N (%); SD = Standard deviation; IQR = Interquartile range; Mann-Whitney-U Test was used for quantitative data, all other p-values result
from a χ2-test for qualitative data (or Fisher’s Test if any cell has an expected cell count less than 5); SPPP = standard pre-scan patient preparation; IPPP = intensified
pre-scan patient preparation; HCC/CCC = Hepatocellular/ Cholangiocellular carcinoma; BMI = Body mass index; TSM = transient severe respiratory motion; CT
CM = CT contrast media; Allergy general = any allergic disposition to substances or food; Cardiac problems = Hypertension, atrial fibrillation, others;
��
= Data was not recorded at site A; significant p-values are depicted in bold.
patients with SPPP (18%; p = 0.401); and site B: 12/58 patients with IPPP (20.6%) vs. 13/52
patients with SPPP (25%; p = 0.590). The TSM incidence in patients with IPPP and SPPP did
not differ significantly between both sites (site A: p = 0.227; site B: p = 0.390). Out of 170
patients without TSM, 100 patients (58.8%) with prior liver DCE-MRI experience yielded sim-
ilar RM grades in all dynamic phases compared to the 70 patients (41.2%) who received their
first liver DCE-MRI (all p�0.092). IPPP did not significantly mitigate RM in comparison to
SPPP in any dynamic phase in these patients (all p�0.072; Figs 3 and 4). IPPP also did not sig-
nificantly mitigate RM in comparison to SPPP in the hepatobiliary phase (p = 0.18).

Fig 4. Boxplots with mean respiratory motion (RM) scores of patients without TSM, receiving either SPPP or IPPP prior
to administration of Gd-EOB-DTPA. The error bars indicate the minimum and maximum RM score and the boxes depict the
interquartile ranges demarcated by median scores. In the Gd-EOB-DTPA group, IPPP did not significantly mitigate RM in
arterial (p = 0.181), portal-venous (p = 0.114) and transitional phase (p = 0.072) in comparison to patients who received SPPP.
Risk factors for Gd-EOB-DTPA-related TSM

Prior episodes of TSM (p = 0.005) and a breath-hold capacity of <17 s during pre-imaging
breath-hold training were associated with the occurrence of TSM (p = 0.025; Table 3).
IPPP and SPPP in Gd-DOTA-enhanced dynamic phase imaging

More patients with moderate ascites were allocated by chance to SPPP (p = 0.048), otherwise
baseline characteristics did not differ significantly between patients allocated to SPPP or IPPP
(all p�0.052; Table 2). The Gd-DOTA group comprised more male patients (p = 0.001), with
higher mean body mass index (BMI; p = 0.013) and cirrhosis (p<0.001) but less malignant
tumors (p<0.001) than the Gd-EOB-DTPA group (Table 2). TSM occurred sporadically in
only 4/202 patients (2.0%; p<0.001). One and three patients with TSM were allocated to IPPP
and SPPP (p = 0.621). 125/198 patients without TSM (63.1%) have had prior liver DCE-MRI.

Table 3. Risk factors associated with Gd-EOP-DTPA-related TSM.
Risk factors No TSM TSM p=

Number of patients 170 40
Gender female 87 (51.2) 20 (50.0) >0.999
male 83 (48.8) 20 (50.0)
Age (years) median (IQR) 61.6 (52.6–73.1) 64.0 (55.9–74.5) 0.283
Tumor etiology HCC/CCC 29 (17.1) 10 (25.0) 0.176
metastasis 80 (47.0) 20 (50.0)
no malignancy 61 (35.9) 10 (25.0)
Prior TSM yes 27 (15.9) 15 (37.5) 0.005
Breath-hold capacity (�17s) � yes 45/58 (77.6) 13/58 (22.4) 0.025
median (IQR) 20 (18.4–20) 20 (16.6–20) 0.100
Pleural effusion yes 12 (7.1) 5 (12.5) 0.256
Ascites yes 14 (8.2) 3 (7.5) 0.878
Cirrhosis yes 28 (16.5) 5 (12.5) 0.535
Lung fibrosis yes 7 (4.2) 2 (5.1) 0.797
Flow rate (mL/s) 1 85 (50.0) 15 (37.5) 0.154
2 85 (50.0) 25 (62.5)
Scan time (s) 17 24 (14.1) 12 (30.0) 0.064
BMI (kg/m2) �� 24.9 (22.3–31.0) 24.8 (22.5–28.0) 0.622
CT CM allergy yes 4 (2.4) 2 (5.0) 0.595
Allergy general �� yes 18/85 (21.2) 4/25 (16.0) 0.333
Cardiac problems �� yes 13/85 (15.3) 7/25 (28.0) 0.100
Categories are presented as N (%); SD = Standard deviation; IQR = Interquartile range; Mann-Whitney-U Test was used for quantitative data, all other p-values result
from χ2-test for qualitative data (or Fisher’s Test if any cell has an expected cell count less than 5); HCC/CCC = Hepatocellular/Cholangiocellular carcinoma;
TSM = transient severe respiratory motion; CT CM = CT contrast media; BMI = Body mass index; Allergy general = any allergic disposition to substances or food;
Cardiac problems = Hypertension, atrial fibrillation, others;
�
= Only data from patients at site B with breath-hold training;
��
= Data was not recorded at site A; significant p-values are depicted in bold.
RM grades were similar in any dynamic phase in patients with and without prior liver
DCE-MRI (all p�0.557). Contrary to the Gd-EOB-DTPA group, IPPP significantly mitigated
RM in all dynamic phases in comparison to SPPP (all p�0.031; Fig 5). Patients who received
IPPP in the Gd-DOTA group showed significantly less RM in the arterial, portal-venous and
transitional phase (all p�0.020) than non TSM patients allocated to IPPP in the Gd-
EOB-DTPA group, whereas RM was similar in both contrast agent groups in patients who
received SPPP (all p�0.081; Table 4).
Discussion
In this bi-institutional study, we strived to investigate if an intensified pre-scan patient prepa-
ration (IPPP) could reduce the frequency of Gd-EOB-DTPA-related TSM and the severity of
RM during liver DCE-MRI. We crosschecked the effects of IPPP in patients who received Gd-
DOTA-enhanced DCE-MRI.
Communication about the significance of dynamic phase imaging for diagnosis and the
effects of RM might differ between institutions and this lack of standardization might contrib-
ute to the variable incidence of TSM. For that purpose, the bi-institutional approach strength-
ens the results of this study. Our rationale was to increase patients’ awareness why it is crucial

Fig 5. Boxplots with mean respiratory motion (RM) scores of patients without TSM, receiving either SPPP or IPPP prior to
administration of Gd-DOTA. The error bars indicate the minimum and maximum RM score and the boxes depict the
interquartile ranges demarcated by median scores. In the Gd-DOTA group, IPPP significantly reduced RM in the arterial
(p = 0.018), portal-venous (p = 0.011) and transitional phase (p = 0.031).
to adhere to breath-hold commands through detailed procedural information analogue to pre-

vious studies conducted to reduce unintentional head or limb movement during MRI [20,21].
Supervised breath-hold training in a standardized way aimed to increase patients’ ability to
cope with breath-holding, train adequate behavior at the onset of dyspnea and potentially
increase breath-hold duration [22].
In our study, the frequency of TSM was lower in the IPPP than in the SPPP group, but with-
out statistical significance. The TSM frequency discovered in our study matched the TSM fre-
quency described previously in the literature [1–8] which corroborates the hypothesis that Gd-
EOB-DTPA acts as a chemo-toxic trigger evoking TSM that cannot be willingly mitigated by
education and training. Our results differ from the results of Gutzeit et al. [18] and Song et al.
[19]. The authors reduced the incidence of TSM from 13% to 0% (4/30 vs. 0/30 patients) [18]
and from 14% to 3.8% (14/100 vs. 3/80 patients) [19] by employing a modified breath-hold
command with several breathing cycles prior to imaging. We speculate that additional

Table 4. RM scores in patients with SPPP and IPPP in the Gd-EOB-DTPA and Gd-DOTA group.
All patients RM score pre-contrast arterial portal venous transitional hepatobiliary

Gd-EOB-DTPA n = 210 Median (IQR) 1.2 (1.0–2.0) 2.0 (1.0–3.0) 1.4 (1.0–2.0) 1.2 (1.0–1.9) 1 (1.0–2.0)
Mean (SD) 1.5 (0.7) 2.2 (1.1) 1.7 (0.9) 1.4 (0.6) 1.4 (0.7)
Range 1.0–4.0 1.0–5.0 1.0–4.0 1.0–4.0 1.0–4.0
Gd-DOTA n = 202 Median (IQR) 1.0 (1.0–2.0) 1.5 (1.0–2.0) 1.0 (1.0–1.5) 1.0 (1.0–1.5)
Mean (SD) 1.5 (0.8) 1.7 (0.9) 1.5 (0.9) 1.4 (0.7) N/A
Range 1.0–5.0 1.0–5.0 1.0–5.0 1.0–5.0
p= 0.272 <0.001 <0.001 0.007 -
Patients w/o TSM

SPPP RM score pre-contrast arterial portal venous transitional hepatobiliary
Gd-EOB-DTPA n = 80 Median (IQR) 1.4 (1.0–2.0) 1.9 (1.0–2.4) 1.4 (1.0–2.0) 1.3 (1.0–2.0) 1.0 (1.0–2.0)
Mean (SD) 1.6 (0.8) 1.9 (0.8) 1.7 (0.8) 1.5 (0.6) 1.4 (0.7)
Range 1.0–4.0 1.0–4.0 1.0–4.0 1.0–4.0 1.0–4.0
Mean (SD) 1.6 (0.8) 1.8 (0.9) 1.6 (1.0) 1.5 (0.8) N/A
Range 1.0–4.0 1.0–5.0 1.0–5.0 1.0–5.0
p= 0.775 0.159 0.081 0.197 -
Patients w/o TSM

IPPP RM score pre-contrast arterial portal venous transitional hepatobiliary
Gd-EOB-DTPA n = 90 Median (IQR) 1.2 (1.0–1.5) 1.4 (1.0–2.0) 1.2 (1.0–2.0) 1.0 (1.0–1.4) 1.0 (1.0–1.3)
Mean (SD) 1.4 (0.6) 1.7 (0.9) 1.6 (0.9) 1.4 (0.6) 1.3 (0.6)
Range 1.0–4.0 1.0–5.0 1.0–4.0 1.0–4.0 1.0–4.0
Mean (SD) 1.5 (0.8) 1.5 (0.8) 1.4 (0.8) 1.3 (0.7) N/A
Range 1.0–5.0 1.0–5.0 1.0–4.0 1.0–4.5
p= 0.231 0.007 0.001 0.020 -
Categories are presented as N (%); SD = Standard deviation; IQR = Interquartile range; RM = respiratory motion; TSM = transient severe respiratory motion;
SPPP = standard pre-scan patient preparation; IPPP = intensified pre-scan patient preparation; N/A = not applicable; significant p-values are depicted in bold.
mechanisms of action aside from training and habituation, as proposed by the authors, might
have been activated through slow deep breathing, such as optimization of oxygenation [23] or
short-term reduction of sympathetic activation and chemo-reflex response [24,25]. Such
mechanisms would not have been targeted with our strategy. In our patient cohort, prior epi-
sodes of TSM were significantly associated with the occurrence of TSM, consistent with other
studies [3,26], whereas other risk factors reported in the literature, such as age [6], gender
[6,7,27] or BMI [5,28,29] were not. We identified impaired breath-hold capacity <17 s during
breath-hold training as an additional risk factor for TSM. Interestingly, IPPP did not signifi-
cantly mitigate RM in any of the Gd-EOB-DTPA-enhanced dynamic phases in patients with-
out TSM, whereas it significantly reduced RM in all dynamic phases in patients who received
Gd-DOTA. This finding implies that Gd-EOB-DTPA-related breath-hold difficulty does nei-
ther affect only the subgroup of patients with obvious TSM nor exclusively the arterial phase,
as proposed in previous studies [1,2,30], but that it affects all dynamic phases albeit to a much
lesser extent. To the best of our knowledge, our study is the first that used such a study design
and yielded these results.
Despite the difficulty to reduce TSM, we want to emphasize that hepatospecific contrast
agents with their unique pharmacokinetic properties cannot be replaced and are still urgently

needed for liver lesion detection and characterization as well as the determination of liver
function. Currently, the most promising strategies to either improve image quality despite
TSM or reduce TSM in the first place, as we anticipated, include the dilution of gadoxetic acid
[15,16] and new acquisition methods to shorten the acquisition time [12,31], acquire multiple
arterial phase images in one single breath-hold [11,12,32] or acquire artifact-free images dur-
ing free breathing [13,33,34]. The results from new acquisition methods are encouraging but
their need for sophisticated hard- and software (parallel imaging techniques: SENSE,
GRAPPA, CAIPIRINHA, VIBE, compressed sensing) still constrains their availability.
Our study had some limitations. First, there was no dedicated randomization for IPPP at
either site, which might have introduced a selection bias. However, it was performed in conse-
cutive patients based on the staffs’ duty in the MRI unit, which constitutes an element of coin-
cidence. Aside from moderate ascites in the Gd-DOTA group, patient characteristics were
similar in all patient groups. Second, there might be a bias by choice of contrast agent at site B,
which, however, was based on site specific SOPs and not influenced otherwise. Third, injection
rate differed between both sites. However, we found no significant association between injec-
tion rate and incidence of TSM, corroborating the results by Ringe et al. [35] but contradicting
the results by Kromrey et al [31]. Here, it is important to mention that there is a huge variation
and considerable overlap of the reported rates of TSM after different injection rates (1 mL/s:
4.8% to 12.9% [5,26]; 2 mL/s: 7.5% to 21.1% [6,8]). Also, some institutions prefer weight-
adapted, others fixed doses of gadoxetic acid making comparisons even more difficult. Fourth,
acquisition time for the dynamic phases differed between both sites with a near significant
association between scan time and TSM (p = 0.064; Table 3). Fifth, the effect of IPPP was mea-
sured only indirectly based on RM image artefacts, which is prone to be biased by subjective
interpretation. Although the inter-reader agreement in our study was very good to excellent
and matched the results of a recent multi-center trial [36], the assessment of IPPP by dedicated
patient questionnaires, respiratory waveform analysis [7,10,14,37,38] or including classifica-
tion of hyper- and hypovascular liver lesions might have added valuable information and
should be addressed in future studies.
Conclusions
In conclusion, IPPP failed to reduce Gd-EOB-DTPA-related TSM and RM in patients without
TSM in comparison to SPPP, corroborating the hypothesis that Gd-EOB-DTPA acts as a
chemo-toxic trigger evoking breath-hold difficulties which cannot be mitigated by these mea-
sures. Interestingly, IPPP, however, seems to be an effective way to mitigate RM in liver
DCE-MRI with extracellular contrast agents such as Gd-DOTA. This suggests that Gd-
EOB-DTPA-related breath-hold difficulty does neither affect only the subgroup of patients
with TSM nor exclusively the arterial phase as previously proposed but rather all patients and
all dynamic phases, albeit to a much lesser extent.
Supporting information
S1 Table. De-identified dataset including scan information, all measured motion scores
and information on presence of potential risk factors for TSM.
(XLSX)
Author Contributions
Conceptualization: Christian Wybranski, Katharina Fischbach.
Data curation: Christian Wybranski, Florian Siedek, Susanne Steinhauser.

Investigation: Christian Wybranski, Florian Siedek, Robert Damm, Angelos Gazis, Ortrud
Wenzel, Stefan Haneder, Thorsten Persigehl, Susanne Steinhauser, Maciej Pech, Frank
Fischbach, Katharina Fischbach.
Methodology: Christian Wybranski, Thorsten Persigehl, Katharina Fischbach.
Project administration: Christian Wybranski, Maciej Pech, Katharina Fischbach.
Supervision: Stefan Haneder, Thorsten Persigehl, Susanne Steinhauser, Maciej Pech, Frank
Fischbach, Katharina Fischbach.
Validation: Susanne Steinhauser.
Visualization: Christian Wybranski, Florian Siedek, Susanne Steinhauser.
Writing – original draft: Christian Wybranski, Florian Siedek.
Writing – review & editing: Christian Wybranski, Florian Siedek, Robert Damm, Angelos
Gazis, Ortrud Wenzel, Stefan Haneder, Thorsten Persigehl, Susanne Steinhauser, Maciej
Pech, Frank Fischbach, Katharina Fischbach.
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26418367

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PLOS ONE

Respiratory motion artefacts in Gd-EOB-DTPA

‡ CW and FS are Joint First Authors to this work.

Citation: Wybranski C, Siedek F, Damm R, Gazis A, Abstract

Copyright: © 2020 Wybranski et al. This is an open Material and methods

PLOS ONE | https://doi.org/10.1371/journal.pone.0230024 March 20, 2020 1 / 16

PLOS ONE | https://doi.org/10.1371/journal.pone.0230024 March 20, 2020 2 / 16

Materials and methods

Standard pre-scan preparation (SPPP)

Intensified pre-scan preparation (IPPP)

Patient allocation to SPPP and IPPP

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referring physicians. Gd-EOB-DTPA was administered intravenously at a fixed dose of 10 mL

PLOS ONE | https://doi.org/10.1371/journal.pone.0230024 March 20, 2020 5 / 16

Table 1. Technical MRI parameters at sites A and B.

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Evaluation of risk factors for Gd-EOB-DTPA-related TSM

IPPP and SPPP in Gd-EOB-DTPA-enhanced dynamic phase imaging

PLOS ONE | https://doi.org/10.1371/journal.pone.0230024 March 20, 2020 7 / 16

Pre-scan preparation: Gd-EOB-DTPA Pre-scan preparation: Gd-DOTA Gd- Gd-DOTA

PLOS ONE | https://doi.org/10.1371/journal.pone.0230024 March 20, 2020 8 / 16

Risk factors for Gd-EOB-DTPA-related TSM

IPPP and SPPP in Gd-DOTA-enhanced dynamic phase imaging

PLOS ONE | https://doi.org/10.1371/journal.pone.0230024 March 20, 2020 9 / 16

Table 3. Risk factors associated with Gd-EOP-DTPA-related TSM.

Risk factors No TSM TSM p=

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to adhere to breath-hold commands through detailed procedural information analogue to pre-

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All patients RM score pre-contrast arterial portal venous transitional hepatobiliary

Patients w/o TSM

Patients w/o TSM

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11. Gruber L, Rainer V, Plaikner M, Kremser C, Jaschke W, Henninger B. CAIPIRINHA-Dixon-TWIST

PLOS ONE | https://doi.org/10.1371/journal.pone.0230024 March 20, 2020 15 / 16

PLOS ONE | https://doi.org/10.1371/journal.pone.0230024 March 20, 2020 16 / 16

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