Reducing respiratory motion artifacts in gadoxetate disodium-enhanced magnetic resonance imaging (EOB-MRI): assessing assisted breath-holding effectiveness

Introduction

Gadolinium-ethoxybenzyl-diethylenetriamine pentaacetic acid (Gd-EOB-DTPA) is a useful hepatocyte-specific magnetic resonance imaging (MRI) contrast agent (1). The primary advantage over other contrast agents is that it can obtain both conventional dynamic contrast-phase imaging and hepatobiliary phase imaging (2,3). This dual functionality enhances lesion conspicuity and the contrast between lesions and the liver, thereby promoting better detection and characterization of focal liver lesions (4,5). Although the hepatobiliary phase offers supplementary information, the enhancement in the arterial phase is still vital for diagnosing hypervascular lesions, particularly hepatocellular carcinoma (HCC) (6-9). However, multiple studies have demonstrated that transient severe motion (TSM) in the arterial phase leads to respiratory motion artifacts, resulting in image degradation and reduced diagnostic accuracy (10-12). Previous studies have reported an incidence of respiratory motion artifacts from 10.7% to 39% (12-16).

The occurrence of respiratory motion artifacts is associated with the shortened breath-hold duration after intravenous administration of gadoxetate disodium. (17). While the exact pathomechanism of TSM is still unknown, several risk factors, such as higher doses of gadoxetate disodium, chronic obstructive pulmonary disease (COPD), and history of TSM, are likely to have an impact on its occurrence (12,14,16,18). There is no consensus on the exact cause of respiratory motion artifacts, but their detrimental effects on image quality are reported in many articles. Suboptimal image quality in the arterial phase may compromise the advantages of hepatobiliary phase imaging with EOB-MRI. Therefore, it is necessary to explore practical strategies to reduce or prevent these artifacts, which are essential for enhancing diagnostic accuracy.

Currently, common strategies for reducing respiratory motion artifacts include reducing injection rate (19-21), diluting contrast agent (20,22), using modified breathing instructions (23,24), and applying multi-arterial phase imaging (16,25-28). However, their routine adoption may be limited by workflow complexity, equipment availability, or the need for protocol customization across institutions. These approaches often require high patient compliance, involve complex operational procedures, and depend on advanced equipment and complicated training.

To overcome these limitations, we propose an assisted breath-holding technique. In this method, a nurse assists the patient in holding their breath in the crucial arterial phase of the imaging process. We hypothesized that brief manual nasal occlusion during the hepatic arterial-phase acquisition could reduce respiratory motion through two complementary mechanisms. First, by transiently occluding nasal airflow, the maneuver may suppress inadvertent nasal inspiration or shallow “reflex” breaths that can occur during attempted breath-holding and are sufficient to introduce arterial-phase motion. Second, the gentle pinch provides an immediate external tactile cue, reinforcing the timing and salience of the breath-hold instruction at the most motion-sensitive phase and thereby supporting breath-hold compliance and stability during data acquisition. We present this article in accordance with the TREND reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1-2127/rc).

Methods

Ethics declaration

The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Medical Ethics Committee of The First Affiliated Hospital of Chongqing Medical University (approval No. 2020-579). Written informed consent was obtained from all participants.

Participants

Patients who underwent EOB-MRI examinations at the Yuanjiagang Branch (Branch A) and Jinshan Branch (Branch B) of The First Affiliated Hospital of Chongqing Medical University between September 2020 and September 2023 were included in the study. The inclusion criteria were as follows: (I) patients able to cooperate and complete the MRI scan; (II) patients demonstrating adequate spontaneous breath-holding capability before the intravenous administration of gadoxetate disodium (a breath-holding score of 3 or above, as described below); (III) adult patients. The exclusion criteria were: (I) patients who had previously undergone EOB-MRI examinations; (II) patients unwilling to continue participating in the controlled experiment; (III) patients with metal implants, who are contraindicated for MRI examinations. The patients who met the inclusion criteria were assigned to consecutive groups, with 309 patients in the control group and 308 patients in the experimental group (Figure 1).

Figure 1 Summary of patients enrollment and exclusion for this study. MRI, magnetic resonance imaging.

Magnetic resonance (MR) examination protocol

Patients at Branch A underwent imaging using the General Electric (GE) 3.0T Signa HDx MRI scanner (USA; 60-cm bore diameter and 70-cm patient-bore length) with a heart-phased coil, while patients at Branch B were scanned using the GE 1.5T Signa HDxt MRI scanner (USA; 60-cm bore diameter and 70-cm patient-bore length) with an abdominal phased coil. Arterial enhancement was achieved using the liver acquisition with volume acceleration-extended volume (LAVA-XV) sequence with centric k-space ordering to collect three-dimensional (3D) T1-weighted images. The scanning parameters of the LAVA-XV sequence are presented in Table 1. Gd-EOB-DTPA (Primovist, Eovist, Bayer-Schering Healthcare, Berlin, Germany) was used and delivered in a 10 mL pre-loaded glass syringe. All electronic injections in the study were performed and recorded using the Medrad Spectris Solaris EP MR Injection System and Injection Logger (Medrad; Warrendale, PA, USA) software. The contrast agent was administered at a dose of 0.1 mL/kg and an infusion rate of 1.0 mL/s without dilution, followed by a 20 mL saline flush at the same injection rate.

All patients received standardized breath-hold training prior to scanning, which included multiple repetitions of inspiratory breath-holding instructions to familiarize them with the command timing and improve compliance. After acquiring the localizer and pre-contrast sequences, arterial phase imaging was initiated. The arterial phase timing was manually determined using a real-time two-dimensional (2D) fluoroscopic triggering method. Upon visual confirmation of contrast arrival in the proximal abdominal aorta on real-time 2D fluoroscopic images, patients were instructed to hold their breath, and image acquisition was immediately commenced.

Breath-hold training standardization

Before imaging, all participants underwent a standardized breath-hold training session conducted by the same trained nursing team using a fixed script. The training consisted of three practice cycles with a target breath-hold duration of 20 seconds per cycle. The verbal commands were identical across groups (“Breathe in… breathe out… hold your breath…” followed by “Breathe normally”) and were delivered with the same timing relative to sequence initiation. The total training time for each participant did not exceed three minutes. To mitigate potential performance bias, nurses were instructed to adhere strictly to the standardized script and timing.

Assisted breath-holding

During arterial phase imaging, patients in the control group underwent scanning using the conventional self-controlled breath-hold technique, as is standard in routine liver MRI protocols. In contrast, patients assigned to the experimental group were subjected to an assisted breath-holding technique. Specifically, before the contrast injection and arterial phase acquisition, trained nurses were pre-briefed and instructed regarding their role in facilitating the patient’s breath control. Once the patient was instructed to “inhale—exhale—hold breath” by the technologist, the nurse stood at the head side of the table and gently pinched both nostrils closed by grasping the bilateral alae nasi between the thumb and index finger (light pressure sufficient to occlude nasal airflow). This manual intervention was maintained throughout the arterial phase image acquisition, and upon hearing the verbal cue “you may breathe”, the assistant promptly released their grip, allowing the patient to resume normal respiration (Figure 2). The maneuver was discontinued immediately if the patient reported discomfort or attempted to breathe.

Figure 2 Assisted breath-holding technique during arterial phase imaging.

For infection control, the assisting staff performed hand hygiene immediately before patient contact and wore disposable gloves during nostril pinching, in accordance with institutional standard precautions and infection-control policy.

Adverse events

Following the MR examination, patients were interviewed by the technologist who conducted the scan to assess post-procedural symptoms. The interview process was minimally structured, consisting of a single predefined question regarding breathing difficulty (e.g., “Did you feel shortness of breath during the breath-hold?”), while avoiding additional leading or suggestive prompts. Responses were recorded as yes/no.

No validated scales were employed to quantify discomfort, anxiety, or procedural acceptability.

Image evaluation

Image evaluation was performed by transferring the images to the Advantage Workstation (version 4.6, GE Healthcare, Chicago, USA) for analysis. Two board-certified MRI radiologists, each with over a decade of post-fellowship experience, independently evaluated the prospectively acquired imaging datasets. Both radiologists possessed extensive expertise in identifying respiratory motion artifacts and distinguishing them from other types of artifacts, such as truncation artifacts. The image review was conducted in a blinded manner, and a respiratory motion score ranging from 1 to 4 was assigned to each imaging phase based on a predefined grading scale (Figure 3): A score of 1 indicated no respiratory motion artifacts; a score of 2 denoted mild respiratory motion artifacts that did not affect the diagnosis; a score of 3 reflected moderate respiratory artifacts that impaired diagnostic accuracy; and a score of 4 represented severe respiratory artifacts that rendered the image non-diagnostic. Scores of 3 or above were classified as an arterial-phase respiratory artifact. In cases where the evaluations of the two radiologists differed, a consensus was reached through discussion to determine the final score.

Figure 3 Respiratory motion artifact scoring criteria. 1 point = no motion artefacts (A); 2 points = mild respiratory motion artifacts (B); 3 points = moderate respiratory artifacts (C); 4 points = severe respiratory artifacts (D).

Statistical analysis

Continuous patient characteristics were described using means and standard deviations, while categorical variables were presented as frequencies. To assess differences in age, body mass index (BMI), and administered contrast dose between the control and experimental groups, independent-sample t-tests were conducted. For the comparison of other categorical variables, including dyspnea, across groups, either the Chi-squared test or Fisher’s exact test was used, as appropriate, based on expected cell counts and sample size. Cohen’s Kappa was used to evaluate the inter-reader agreement of image evaluation. Interpretative benchmarks for Kappa values are as follows: scores between 0.0 to 0.20 suggest only slight agreement; values from 0.21 to 0.40 reflect fair agreement; scores in the range of 0.41 to 0.60 indicate moderate agreement; those between 0.61 and 0.80 demonstrate good; and values exceeding 0.80, up to 1.00, denote near-perfect to perfect consensus among evaluators.

All statistical analyses were performed using the SPSS 22.0 software package. A two-tailed P value less than 0.05 was regarded as statistically significant. All tabulated values were generated from the locked dataset to prevent transcription discrepancies.

Results

The demographic characteristics of the participants in both the control and experimental groups were similar. A total of 617 patients were enrolled in this study, comprising 309 (100 females, 209 males) in the control group and 308 (102 females, 206 males) in the experimental group. The mean age of patients was 55.63±11.21 years in the control group and 55.17±12.13 years in the experimental group. There were no significant differences between the two groups in terms of sex, age, BMI, or contrast agent dosage (P>0.05, Table 2).

The incidence of self-reported dyspnea was similar between the groups. In the control group, 6 out of 309 participants (1.94%) reported experiencing dyspnea, while 8 out of 308 participants (2.60%) in the experimental group reported the same. Statistical analysis revealed no significant difference between the groups (χ²=0.30, P=0.58).

Reader 1 and Reader 2 showed similar overall patterns between the control and experimental groups. The reader-specific distributions of artifact grades by study group are summarized in Table S1. For Reader 1, the overall 4-category distribution differed significantly between groups (χ²=60.01, P<0.01). Similarly, for Reader 2, the overall distribution also differed significantly (χ²=34.27, P<0.01). Inter-reader agreement for the four-level ordinal scale was excellent [Kappa =0.84, P<0.01, 95% confidence interval (CI): 0.80–0.87].

Inter-reader agreement for image quality parameters was good (Kappa =0.68, P<0.01, 95% CI: 0.65–0.71). The distribution of arterial-phase artifact severity was: none artifacts (142, 45.95%), mild artifacts (109, 35.28%), moderate artifacts (32, 10.36%), severe artifacts (26, 8.41%) in the control group; and none artifacts (231, 75.00%), mild artifacts (61, 19.80%), moderate artifacts (12, 3.90%), severe artifacts (4, 1.30%) in the experimental group. These findings are detailed in Table 3.

Discussion

In this study, we analyzed data from 617 patients who underwent EOB-MRI at two independent sites. Our findings show that the assisted breath-holding technique significantly reduces the incidence of moderate-to-severe respiratory motion artifacts during the hepatic arterial phase, without significantly increasing self-reported dyspnea assessed immediately after the scan. This simple and feasible technique provides an effective solution for reducing respiratory artifacts and improving image quality during the arterial phase, making it a practical approach for routine clinical applications. By incorporating assisted respiratory control, this method aims to reduce motion artifacts and improve image quality during the critical arterial phase, which is highly sensitive to respiratory motion.

Previously reported incidence rates of respiratory motion artifacts have varied from 10.7% to 39%, depending on the study population and MRI examination protocol (12,19,22,25,29). We used a widely accepted standard protocol with an injection rate of 1 mL/s to ensure optimal visibility of lesions and contrast between lesions and the liver. Our study found that 18.8% (58/309) of the control group experienced respiratory motion artifacts after receiving gadoxetate disodium, which falls within the range of previous reports Haradome et al. (19) reported a similar result of 18.5% (20/108) using the same MRI acquisition technique as our study (a slow injection rate of 1 mL/s and MR fluoroscopic triggering technique). Gruber et al. (25) also reported a comparable initial incidence of 18.9% using an injection rate of 1.5–2.0 mL/s and single arterial volumetric interpolated breath-hold examination (VIBE). Employing an optimized acquisition sequence to achieve multi-arterial phase acquisition reduced this incidence to 7.8%. In contrast, our study achieved a lower rate of 5.2% (16/308) by utilizing the assisted breath-holding technique. This highlights the effectiveness of our method in mitigating respiratory motion artifacts without the need for high-end equipment.

A number of optimization techniques have been investigated in recent years in an effort to lower the frequency of respiratory motion artifacts. Besides multi-arterial phase acquisition, other technical methods have been explored to reduce respiratory motion artifacts, including deep learning algorithms (30), free-breathing protocols (31,32), and acceleration acquisition techniques with brief breath-hold times (25,33). However, these advanced acquisition methods require complex hardware and software that may not be available in every institution. Strategies that can be easily implemented to lower the incidence of artifacts are desperately needed. Another previously described method for minimizing respiratory motion artifacts is to adjust the gadoxetate disodium injection protocol. Polanec et al. (20) and Kim et al. (22) reported that 1 mL/s (20) or 1:1 dilution of gadoxetate disodium at an injection rate of 2 mL/s (22) notably decreased the incidence. In many institutions equipped with dual-head injectors, saline chasers and dilution protocols can be implemented efficiently under standard aseptic practice. Practical considerations more commonly relate to protocol complexity, local workflow, and additional consumables/cost rather than inherent contamination risk. Modified breathing instructions were another recently reported strategy that decreased the incidence of TSM from 33.3% to 16.7% (23). However, the training process can be time-consuming and laborious, and this approach depends on patient cooperation. Unlike previous research, our assisted breath-holding technique used less complicated methods to achieve a relatively low respiratory motion artifact rate.

The inability to finish the breath-holding and a reduction in the maximum breath-holding duration are the two ways that the degradation of breath-holding capacity following an intravenous injection of gadoxetate disodium manifests, according to a study by McClellan et al. (17). The former had an incidence of 80% (35/44) while the latter had an incidence of 27% (12/44). Our assisted breath-holding technique may help improve breath-hold stability in patients who can perform breath-holding but have difficulty maintaining consistent breath-hold during arterial-phase imaging. The main reason for its effectiveness is that giving these patients external support for pinching their noses can extend the time they can hold their breath, ensuring that high-quality images are captured during the vital arterial phase of imaging.

Respiratory motion artifacts’ precise etiology and pathophysiology are still up for debate. Davenport et al. (15) first proposed that subjective sensations of dyspnea might cause the diaphragm to move, which would produce respiratory motion artifacts. However, Motosugi et al. (11) found that breath-holding failure, not dyspnea or SpO2 drops, was the primary cause of arterial-phase artifacts following gadoxetate disodium administration. According to our research, only 1.9% (6/309) of patients reported having dyspnea, whereas 18.8% (58/309) of arterial-phase images displayed moderate-to-severe respiratory motion artifacts. This discrepancy challenges Davenport’s hypothesis. Our research findings respond to viewpoints proposed by Motosugi and colleagues. The assisted breath-holding technique uses outside help to lower the rate of breath-holding failure.

The innovative aspect of the assisted breath-holding technique lies in its conceptual simplicity and integration within existing contrast-enhanced MRI workflows, rather than in the introduction of new hardware or complex procedural modifications. By providing external assistance during the breath-hold, this approach can prolong effective breath-holding and thereby reduce the incidence of respiratory motion artifacts without requiring additional equipment or protocol restructuring.

In our clinical setting, the technique was implemented by nursing staff who routinely participate in respiratory coaching and contrast-enhanced MRI examinations, and therefore did not necessitate additional personnel or changes in staffing structure. However, it should be acknowledged that this approach increases nursing workload during the arterial-phase acquisition, which may influence its practicality in high-throughput environments.

Several limitations of this study should be acknowledged. Firstly, we extensively included patients who could cooperate and complete the EOB-MRI scan without considering other factors that might affect the degree of arterial enhancement. As a result, we are unable to draw any conclusions from our data regarding whether underlying diseases influenced the results of breath-holding ability or caused bias. Second, technologists could not be blinded to the intervention, which may introduce performance bias despite the use of a standardized coaching script and fixed timing cues; this limitation should be considered when interpreting the observed effect size. Third, although data were collected from two branches using different scanners (3T vs. 1.5T) and acquisition protocols, we did not perform branch- or scanner-stratified analyses; therefore, field-strength–related as well as scanner- and center-related heterogeneity in baseline artifact rates and in the magnitude of the intervention effect cannot be excluded. Fourth, patient experience was not assessed using validated quantitative instruments (e.g., Visual Analog Scale for discomfort or Likert-based acceptability/anxiety scales). Fifth, excluding patients with prior EOB-MRI experience and enrolling only participants who demonstrated baseline breath-holding capability may have biased the cohort toward lower-risk individuals, thereby limiting the external validity and generalizability of our findings to higher-risk populations. Finally, this method may not apply to patients with nasal diseases, traumatic brain injury, or extreme anxiety. However, more research is required to determine the efficacy of this approach in patients with respiratory distress (such as COPD or other lung diseases).

Conclusions

The application of the assisted breath-holding technique can significantly reduce respiratory motion artifacts in EOB-MRI without significantly increasing self-reported dyspnea. By addressing a critical limitation of EOB-MRI, this approach supports enhanced hepatobiliary imaging and sets the stage for future advancements in motion artifact mitigation techniques.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the TREND reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1-2127/rc

Data Sharing Statement: Available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1-2127/dss

Funding: This work was supported by the Foundation of Disciplinary Advancement Cultivation Project (No. XKTS150).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-2025-1-2127/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by the Medical Ethics Committee of The First Affiliated Hospital of Chongqing Medical University (approval No. 2020-579). Written informed consent was obtained from all participants.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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