Is whole‐body magnetic resonance imaging a source of anxiety in oncological patients?

Abstract Objective Magnetic resonance often produces feelings of anxiety before, or during, the examination. The aim of this study was to assess anxiety and potential causes of anxiety in cancer patients undergoing whole‐body magnetic resonance imaging (WB‐MRI). Methods This monocentric study recruited 70 cancer patients who were scheduled to undergo WB‐MRI for detection, staging or therapy monitoring. At baseline (prior to the WB‐MRI), assessments were performed using the State–Trait Anxiety Inventory (STAI‐Y 1), Illness Perception Questionnaire (IPQ‐R), Big Five Inventory (BIF‐10) and Revised Life Orientation Test (LOT‐R), while at the end of the WB‐MRI examination the patients repeated the STAI‐Y 1 questionnaire and were asked to indicate their preference between WB‐MRI and computed tomography. Results We found a positive correlation between pre‐ and post‐examination STAI‐Y 1 scores (r = 0.536, p < .0001), with no significant difference between them. Pre‐examination STAI‐Y 1 scores had a negative correlation with the emotional stability in the BIF‐10 questionnaire (r = −0.47, p = .001) and a positive correlation with emotional representation (r = 0.57, p = .001) in IPQ‐R. The post‐examination STAI‐Y 1 had a negative correlation with optimistic orientation (r = −0.59, p = .001). Conclusions The anxiety associated with a WB‐MRI examination was only in small part associated with the examination itself, and in fact, most patients preferred WB‐MRI to computed tomography. Concern with the outcome of the examination was likely a greater source of anxiety.

and cancer-prone syndromes (Li-Fraumeni, 8 hereditary paraganglioma and pheocromocytoma syndromes 9 ). Moreover, this exam is also widely used for the staging and follow-up of other cancer histotypes and cancer related syndromes (including breast cancer, 10 lymphoma, 11 neurofibromatosis 12 and Von Hippel Lindau Syndrome 13 ). It is also commonly applied when standardized investigations have yielded inconclusive results, 14 and in pregnant cancer women in need of accurate systemic staging. 15 WB-MRI allows the detection of small lesions throughout the body 16 without the need for exposure to ionizing radiation and in most cases without the injection of contrast agents, thus avoiding their associated risks. 17,18 Moreover, WB-MRI has a diagnostic performance equal to total-body computed tomography (CT) with contrast agent or positron emission tomography (PET). 19,20 The combination of comparable performance and the non-presence of risks from radiation exposure and contrast agent injection posed the WB-MRI as a good alternative by radiologists for whole-body examination of eligible patients. 21 The literature shows however, that patients report discomfort and anxiety during magnetic resonance examinations and these factors can lead to the procedure being a stressful experience. A review investigating the relationship between anxiety symptoms and magnetic resonance imaging 22 demonstrated that up to 30% of patients reported high levels of worry, while 5%-10% of patients showed severe psychological problems. The situation may be even more severe, as, Oliveri et al. 23 found that 93.6% of patients who had previously undergone an MRI examination reported at least a medium level (M = 3.8 on a VAS scale) of anxiety and concern related to the examination.
In oncological patients, anxiety and concern arise in a context already charged with the fear of death and uncertainty: the need to control the disease and its prognosis often arise among patients despite cancer characteristics. 24 Moreover, patients focusing on the negative consequences of the disease showed greater levels of anxiety. Conversely, Downe-Wamboldt et al. 25 have provided evidence that a favorable illness perception can allow a better comprehension of the disease, thus favor more effective coping strategies in cancer patients.
To the best of our knowledge, few qualitative studies investigating the experiences of patients undergoing an WB-MRI examination have been conducted and only two studies have qualitatively explored patients' and subjects experience, acceptance and anxiety with WB-MRI. 23,26,27 The aim of this study was to assess anxiety with the State-Trait Anxiety Inventory (STAI-Y 1) 28 questionnaire and investigate potential factors affecting pre-and post-exam anxiety in cancer patients undergoing whole-body magnetic resonance imaging (WB-MRI).

| METHODS
This was a prospective study that examined the associations of breast and prostate cancer patients' disease perception, personality dimensions, and optimistic orientation with anxiety in the context of WB-MRI.

| Participants and procedure
Seventy oncological patients (46 Breast cancer; 24 Prostate cancer) undergoing WB-MRI for staging and therapy monitoring were prospectively enrolled to this institutional review board approved study (1032_UID_1810) between June 2020 and November 2020. Written informed consent was obtained from all subjects involved in the study.
Participants included in the study were cancer patients with metastatic (stage IV) disease who were undergoing WB-MRI based on an oncologist's recommendation with no contraindication to the MRI examination (e.g., pacemaker, pregnancy in the first trimester). Exclusion criteria were anxiety disorder and psychological or pharmacological treatments for anxiety.
Participants were recruited before the WB-MRI, while they were waiting for the examination. After providing informed consent, the participants were invited to meet the psychologist for psychological assessment and collection of sociodemographic and medical characteristics, including gender and age.
The following measures were included in the psychological assessment: • The State-Trait Anxiety Inventory subscale (STAI-Y 1), 28 which was the only questionnaire administered both before and after the WB-MRI examination. It is a self-report questionnaire composed of 20-items having scores ranging from 1 to 4, with higher score indicating higher state anxiety levels.
• The Revised Life Orientation Test (LOT-R) 29 was administered before the WB-MRI examination to measure the optimistic orientation. It is a self-report questionnaire of 10 items that measures the optimism or pessimism of people's attitude toward the future.
Scores for each item range from 0 to 4, with a higher total score in the sum of the items indicating more optimism.
• The 10-item Big Five Inventory (BIF-10) 30 was used before the WB-MRI examination to assess personality traits (agreeableness, conscientiousness, emotional stability, extroversion, and openness). It is a self-report tool composed of 10 items, with scores ranging from 1 to 5.
• The Illness Perception Questionnaire (IPQ-R) 31 was also administered before the WB-MRI examination to assess the patients' perception of illness. The questionnaire is composed by three sections: the identity subscale (assensing symptoms the patient associates with the illness), the causal subscale (measuring personal ideas about etiology), and a third section including different subscales on acute/chronic and cyclical timeline (the perceived duration of the illness), consequences (the expected effects and outcome), treatment control (how one controls or recovers from the illness), disease coherence, and emotional representations. It is a self-report questionnaire with scores ranging from "strongly disagree" to "strongly agree".
To evaluate the preferences about imaging technique, after the WB-MRI examination the patients were asked to indicate which examination they preferred between WB-MRI or CT. More specifically, patients answered the following question:" "If you had to repeat these tests in the future, would you choose CT or WB-MRI?".
We note that the contexts of CT scans for the patients included both whole-body examinations (with or without PET scan) for staging purposes, and local scans for treatment planning. In the former case, an injection is required either a PET radiotracer, or CT contrast agent depending on the specific examination undertaken. Whereas

| Demographic characteristics of study sample
The 70 participants had a mean age of 60 years (range 37-82 years), 66% of patients were female with breast cancer, and 34% were male with prostate cancer. As regards education, 56% had graduate, 31% high school, and 13% middle school levels of education (Table 1).

| Correlation and regression analysis
A positive correlation was found between pre-and post-examination STAI-Y 1 scores (r = 0.536, p < .001). There was however, no significant difference between the pre-and post-examination STAI-Y 1 scores (Table 2).
The pre-examination STAI-Y 1 was positively correlated with the emotional representation subscale score (r = 0.57, p = .001), timeline Age did not have a significant effect on personality traits, dispositional optimism or illness perception.

| Preferences of imaging technique
Of the 70 participants, 55 preferred WB-MRI; 5 preferred CT, and 10 did not indicate a preference.

| DISCUSSION
With the patient-centered approach being of growing importance to oncology care, there are many aspects to everyday practice that require consideration of the patient's perspective, preferences and interests. In the present study, we examined the associations of breast and prostate cancer patients' disease perception, personality dimensions, and optimistic orientation with their anxiety in the context of WB-MRI.
We found a positive correlation between pre-and post-WB-MRI examination levels of anxiety, but no significant difference between them. We attribute the lack of significant difference to the fact that the patients had not yet received the examination report, and therefore the context was not resolved, when compiling the postexamination STAI-Y 1. This view is motivated by the findings by Oliveri et al. 24 that the main concern reported by patients before undergoing a WB-MRI examination was not related to the examination itself, but to the outcome, that is: the possibility of discovering the presence of cancer. Similarly, Katz et al. 32 have found that along with the fear of pain, the expectation of the test results contributes to examination anxiety. Moreover, it is consistent with the correlation we found between pre-examination anxiety and the "timeline", that lead some patients to experiencing feelings of concern, discomfort to MR examinations. [33][34][35] Indeed, these are sometimes so severe that patients experience their first claustrophobia attack during an MRI examination, even without a previous condition, 32   post-WB-MRI assessment, and given the relatively high correlation between the pre-and post WB-MRI levels of anxiety, it is unsurprising that factors related to disease perception (emotional representation) had a similar, positive association with anxiety before and after the WB-MRI examination. Consistent with Zhang and colleagues (2016) 37 who showed that a more negative emotional representation can be expected to drive negative emotional states; we saw illness perceptions and stress to be associated with the patients' anxiety. Elsewhere, it has been seen that illness perceptions play a significant role in emotional distress experienced by people with low-grade brain tumors, 38 but did not play a significant role in positive affect.
Interestingly, the regression model showed none of the personality characteristics to predict patients' anxiety experienced before the examination. Indeed, the only significant predictors were factors associated with patients' illness perception. In particular, independently of the type of cancer, the patients who were the most concerned about their disease (measured by emotional representation subscale), and were less able to make a sense of the disease (measured by disease coherence subscale), had a higher probability to experience high level of anxiety.

ACKNOWLEDGMENTS
IEO, the European Institute of Oncology, is partially supported by the Italian Ministry of Health (with "Ricerca Corrente" and "5Â1000" funds).

ETHICS STATEMENT
The present study was approved by the IEO Ethics Committee (Trial ID IEO1032).

FUNDING INFORMATION
This study was funded by FIEO-CCM. This work was partially supported by the Italian Ministry of Health with Ricerca Corrente and 5 Â 1000 funds.

CONFLICT OF INTEREST
The authors have stated explicitly that there are no conflicts of interest in connection with this article.