Somatic Distress, Mental Health and Psychological Resilience Among Cancer Patients During the Pandemic: A Cross-Sectional Study

Objective The current researches during COVID-19 have not yet addressed somatic distress among cancer patients. The aims of this study are to investigate the somatic distress and psychological symptoms levels of cancer patients, and analyze the inuencing factors on somatic distress during the pandemic. Methods This cross-sectional study included consecutively selected 216 eligible cancer patients. The Patient Health Questionnaire-15, Posttraumatic Stress Disorder (PTSD) Checklist for DSM-5, The Depression, Anxiety and Stress Scale-21, the Brief Resilience Scale, the Stressful Life Events List due to Pandemic and, demographic and clinical characteristics form were administered to the participants with face to face interviewing.


Introduction
Corona Virus Disease 2019 (COVID-19) has been detected for the rst time in December 2019 in Wuhan, China as a novel pneumonia causing respiratory tract infection. 1  , indicating person-to-person transmission and an asymptomatic course has rapidly spreaded out to the whole world. 2 Most people infected with the Covid-19 virus have been experienced mild to moderate respiratory syndrome and have been recovered without special treatment. Developing serious consequences is a greater risk for the elderly, those with underlying medical conditions such as cardiovascular diseases, diabetes, chronic respiratory issues, and cancer. 3,4 The COVID-19 pandemic has created an unprecedented change in the lives of people worldwide, especially in patients with chronic diseases. Those with cancer may be particularly vulnerable to more severe disease due to their immunocompromised status from the underlying malignancy itself, as well as decreased immunity from cancer-directed treatments, additional medical comorbidities, and poor nutritional status. 5 A few recent studies that evaluated psychological symptoms in oncology patients during the COVID-19 pandemic. 6-9 occurrence rates for depression and anxiety ranged from 9.3-31.0%and from 8.9-36.0%, respectively. 6-8 In a study conducted on 187 oncology patients have been reported, rate of with probable post-traumatic stress disorder (PTSD) 31.6%. 9 Somatic distress has not been investigated yet in cancer patients during the pandemic. Somatic distress presentation in cancer is a complex area because of the overlapping of physical disease and treatment-related mechanisms and possible psychosocial mechanisms, and it is that needs investigation. 10 Previous studies have shown that heightened distress levels can lead to adverse outcomes in cancer patients including decreased satisfaction with care and noncompliance with treatment, low survival rates, desire to accelerate death, and poor quality of life for both patients and their relatives. 11,12 Looking at the new, unrecognized and early unpredictable and uncontrollable pandemic process, it may be much more intense than the stress factors in daily life, it creates a common threat perception, there is a lack of information about the process, it includes social isolation and quarantine processes, in addition to the fact that there is uncertainty about the future, social and economic effects are evident, it is observed that it is distinguished by the fact that it creates a massive stress all over the world. 13 It can be thought that the special population such as cancer patients will be affected more by this mass stress and its effect on them may cause more severe consequences. Therefore, it will be of great importance to de ne the psychological symptoms that may occur in cancer patients during the pandemic. For these reasons, this study aimed to a) estimate the levels of somatic, PTSD, depression, anxiety, and stress symptoms and b) investigated the relationship between somatic distress and demographic characteristics, psychological symptoms, stressful life events, and psychological resilience among the cancer patients during the pandemic. In this way, we aimed to shed light on the measures to be taken to prevent somatic distress and worse mental problems of cancer patients during the pandemic.

Sample and procedure
This cross-sectional study was conducted in University of Health Sciences, Bagcilar Research and Training Hospital, Medical Oncology Clinic and Chemotherapy Unit, between 15 June and 15 October 2020. This study included consecutively selected 216 eligible cancer patients, who receiving treatment or visiting the oncology center for routine follow-up examinations. To be eligible for study participation, patients had to be (a) diagnosed with any cancer type, (b) aged between 18 and 75 years, (c) able to complete questionnaire in Turkish language, and (d) able to provide informed consent. Reasons for exclusion were pregnancy, illiteracy, substance abuse, declared inability to complete questionnaires, serious psychiatric disorders that hindered judgement, and patients with any issues interfering with giving informed consent. The aim of the study was explained to the participants and invited to voluntarily participate, and informed consent forms were obtained before they were included in the study. This research was approved by the University of Health Sciences, Bagcilar Research and Training Hospital's ethical committee (reference 2020.06.1.11.082) and was conducted in accordance with the Declaration of Helsinki. The study protocol was also approved by the Turkish Ministry of Health, General Directorate of Health Services (reference ES-2020-05-07T13_40_22). The Patient Health Questionnaire-15 (PHQ-15), Posttraumatic Stress Disorder Checklist for DSM-5 (PCL-5), The Depression, Anxiety and Stress Scale-21 (DASS-21), the Brief Resilience Scale (BRS), the Stressful Life Events List due to Pandemic and, demographic and clinical characteristics were administered to the participants with face to face interweaving by author XXX who senior social worker trained for the study.

Measures
Demographic and clinical characteristics form.
Age, gender, marital status, education, employment status, economic well-being, comorbidity (hypertension, diabetes, coronary heart disease, chronic obstructive lung disease, chronic kidney disease, and other), and history of psychiatric disorders were assessed via self-report. Clinical characteristics included type of cancer, time since diagnosis, types of treatment currently or previously received, present treatment, and metastasis; this information was obtained from participants' medical charts.
Stressful Events List due to Pandemic.
The scale was prepared by authors, using the Stressful Life Events Screening Questionnaire 14 and review of the literature, and used to measure the stressful life event burden during the pandemic. The scale, answers are 0-no, 1-yes consisting of 18 questions and total scores ranging from 0 to 18. Higher scores on the scale are associated with stressful event burden. Cronbach's alpha internal consistency coe cient was determined as 0.73. A positive and signi cant relationship was found between the total score of the scale and depression (r = .35), anxiety (r = .32), stress (r = .32), PCL-5 total score (r = .41), and PHQ-15 total score (r = .38) (see Supplementary Table 1).
Somatic symptoms were measured using the PHQ-15 scale, which includes the 15 most common somatic symptoms. This scale assesses how much participants were bothered by health symptoms such as "abdominal pain", "back pain" on a scale of 0=not bothered at all to 2=bothered a lot. A total somatic symptom score was calculated, with possible scores ranging from 0 to 30, and scores scaled to account for the additional item asked only of female participants relating to menstrual pain and problems. Higher scores on the PHQ-15 are strongly associated with somatic symptoms. Somatic symptom severity were calculated in four categories based on the PHQ-15 score 'minimal' (0-4), 'mild' (5)(6)(7)(8)(9), 'moderate' (10)(11)(12)(13)(14), or 'severe' (≥15). 15 The Turkish validity-reliability study was conducted by Yazıcı Güleç et al. (2012). 16 In this study, Cronbach's alpha of the PHQ-15 was 0.86.
The PCL-5 is a 20-item measure that assesses PTSD symptomatology: intrusions, avoidance, negative alterations in cognitions and mood (NACM), and hyperarousal. Participants responded to the items on 5point Likert-type scales (0 = not at all to 4 = extremely) in relation to their experience of COVID-19 outbreak, with total scores ranging from 0 to 80. 17 . The Turkish version of PCL-5 was used, which has been shown to be reliable and valid. In this study, used ≥47 as a cut-off point to diagnose possible PTSD. 18 Among the current sample, the PCL-5 and subscales evidenced a Cronbach's alpha of α=.96 for PCL-5, α=.89 for intrusions, α=.87 for avoidance, α=.91 for NACM, and α=.92 for hyperarousal.
The BRS includes six items. The respondents were asked to indicate how well each statement described their behaviour and actions on a 5-point Likert-type scale, ranging from "1" = does not describe me at all to "5" = describes me very well. As Item 2 (I have a hard time making it through stressful events), Item 4 (It is hard for me to snap back when something bad happens) and Item 6 (I tend to take a long time to get over set-backs in my life) were reverse-coded, the data collected were recoded prior to analysis. High scores obtained from the scale after the items coded in reverse order are translated in the scale indicate high psychological resilience. 22 The factor loads for the items were found between 0.68 and 0.91 in Turkish sample. 23 In this study, Cronbach's alpha of the BRS was 0.69.

Statistical analyses
Descriptive statistics were presented in median values and interquartile ranges (IQR) (25% to 75%) for the quantitative variables, and frequencies and percentages for the categorical variables. Normality tests were carried out by using one-sample Kolmogorov-Smirnov and Shapiro-Wilk tests and through histogram graphs. The Mann-Whitney U test was utilized for comparing the continuous variables among two groups. Kruskal-Wallis test was used to evaluate possible differences between the more than two groups and the level of signi cance was determined after the Dunn multiple comparison tests with Bonferroni correction test. Multiple linear regression model was used with backward elimination technique to investigate potentially predictive factors for the somatic distress. The variables evaluated were determined as signi cant variables derived from our results and literature review, in accordance with clinical experience. The variables used for the models are as follows; age (years), gender, education levels

Sociodemographic and clinic characteristics
The demographic-clinical characteristics of participants are summarized in Table 1 Analyzes of association between demographic-clinical characteristics and stressful life events, BRS, somatic distress, PTSD, depression, anxiety, and stress symptoms were given in Supplementary Table 2  and Table 3.
Stressful life events list due to the pandemic The median of stressful life events due to the pandemic that the participants experienced was 3 (IQR= 1 to 5) ( Table 3). Among 216 patients were 9 (4.2%) diagnosed with COVID-19, 7 (3.2 %) hospitalized, and reported are summarized in Table 2.

Discussion
The current researches during COVID- 19 have not yet addressed somatic distress among cancer patients.
The aims of this study are to investigate the somatic distress, PTSD, depression, anxiety, and stress levels of cancer patients whom already vulnerable population, and analyze the in uencing factors on somatic distress during the pandemic. Main ndings of this study; among the cancer patients moderate to severe somatic distress rate was % 38 and probable PTSD rate was 20.4%. Depression, anxiety and stress symptoms were 36.1%, 49.1% and 45.4%, respectively, from mild to extremely severe at any level. There were substantial association between somatic symptoms severity and high PTSD, anxiety, depression, and stress symptoms levels. Low educations levels, high anxiety levels, high experience stressful life events, and low psychological resilience predicted high somatic distress levels.
While the evidence of the psychological effects of the COVID-19 pandemic on the general population continues to increase, studies investigating the effects on special and sensitive populations such as cancer patients are gaining momentum. One of the rst studies from China, Wang et al. showed that among 6213 cancer patients, 17.7% had anxiety, 23.4% had depression and 9.3% PTSD symptom. 7 Chen et al. reported that fear of disease progression, anxiety (16.5%) and depression (28.8%) was much higher in cancer patients under the COVID-19 outbreak than in the general population and then the cancer patients in times without an outbreak. 24 Juanjuan et al found that patients with breast cancer had high rates of anxiety, depression, distress, and insomnia in the peak time of the COVID-19 pandemic. 6 Unlike Musche et al found that 150 cancer patients under treatment had similar levels of distress and anxiety to healthy controls during the rst days of the pandemic, but cancer patients had more adherent safety behavior. 25 Similar to the majority of those studies, it is seen in our study that patients had high level of anxiety and stress insomuch that they were more afraid of catching COVID-19 (39%) or not being able to access treatment on time (38%) because of pandemic than the cancer recurrence (31.5%) in our study. Schellekens et al. also showed that patients were most afraid of being infected with COVID-19 (50.5%) and requiring treatment in the intensive care unit (58.0%). 26 To our knowledge, the current study is the rst to address COVID-19-related PTSD, depression, anxiety, stress, as well as somatic symptoms (using PHQ) in cancer patients. We found only one study that has closely examined somatic symptoms' association with depression, anxiety and PTSD, focusing solely pain and fatigue as somatic symptoms. 7 However, anxiety and stress, which cause aggravation of somatic symptoms such as pain or fatigue, is a well-studied area. 10,27 Somatic symptoms have already been reported in past pandemics even in general population and psychosomatic responses to these psychological effects should be considered. 28 Based on this phenomenon, Chaturvedi reported his prediction of the prevalence of chronic pain and the severity of the pain experience may have increased during the COVID-19 pandemic process. 29 Wang et al. evaluated only physical fatigue and pain intensity as somatic distress in cancer patients using the Visual Analogue Scale (VAS) in their study. They found that pain intensity was a risk factor for anxiety, depression and PTSD. 7 We also found a signi cant relationship between the severity of somatic symptoms and the levels of anxiety, depression, PTSD and stress symptoms. The fact that patients with high anxiety levels, high stressful life events experience, and low psychological resilience seem most vulnerable to somatic distress among cancer patients' is another signi cant result of this study.
Anxiety, depression and PTSD is associated with somatic symptoms. 30,31 It is thought that the somatic sensory processing mechanism extends to cognitive symptoms and reveals a potential generalization of the impairment in the cognitive and somatic domains in PTSD. 31 In line with this, it is seen that 'negative alterations in cognitions and mood' are high in severe somatic distress in PTSD symptomology like other symptomatologies in this study. The COVID-19 outbreak, like other pandemics, was associated with a wide range of psychiatric comorbidities, including anxiety, panic, depression and trauma-related disorders. As a result, cancer patients may be experiencing more somatic distress after all these stressful life events, uncertainty and anxiety during this COVID-19 pandemic.
Psychological Resilience is the ability of an individual to adapt to and cope with adverse situations such as a trauma, threat, health issues. 32.33 Resilience is protective against some mental disorders such as anxiety and PTSD while low psychological resilience is risk factor for mental disorders. 34 Ran et al. showed that psychological distress was high at the peak level of COVID-19 outbreak in China, and was negatively correlated with resilience in the general population. 35 Kimhi et al. showed that individual resilience and well-being were the rst and most important predictors of COVID-19 related anxiety. 36 Kavcic et al. suggested that resilience is of great importance factor that promotes good psychological functioning during COVID-19 outbreak. 37 When these studies are considered together, it is an expected result that high anxiety and low psychological resilience also predict somatic distress in cancer patients during the COVID 19 process.
There are studies that report that less education is associated with greater somatic symptoms. 38, 39 However, Sayar et al. reported that low education level predicted somatic symptoms due to comorbidity with depressive symptomology. 38 Zeleke et al, on the other hand, showed that low education was associated with somatic symptoms in traumatic individuals. 39 So Somatic symptoms may be more apparent in people with low education due to the overlap of COVID-9 stress in cancer patients who are already under own disease stress.

Study limitations
There are several limitations in this study. First, because its cross-sectional design, a cause-effect relationship in variables cannot be established. Whereas, knowing the pre pandemic situation could enable us to reveal the results more clearly. It is a limitation that self-assessment scales were used and additional psychopathologies were not able to screen with a structured interview like SCID. To better understand the impact of COVID-19 on cancer patients as well as somatic distress, large scale studies within the framework of longitudinal and prospective designs are needed.

Clinical implications
This study reveals a high risk of PTSD, depression, anxiety, stress and also somatic distress in patients with various cancer types during the COVID-19 pandemic. Outbreaks and psychological consequences of the outbreak in cancer patients and low psychological resilience may predict high somatic distress in this already vulnerable population. So the implementation of mental health screening and psychosocial approaches to increase psychological resilience for all patients with cancer diagnosis, especially with high somatic symptom levels has a strategic importance.

Conclusions
This study focused on the psychological outcomes of the COVID 19 outbreak in cancer patients and its relation to somatic distress, which is already a gap in the literature. The results showed that the symptoms of depression, anxiety, stress, and PTSD increased, as well as somatic distress. Moreover, indicators predicting somatic distress were determined as; ''low education levels, high anxiety levels, experience of high stressful life events and low psychological resilience'', for which preventive measures should be planned in future studies.

Declarations
The data sets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Authors' contributions E.S., Ö.S., E.K., made substantial contributions to the conception and design of the work. Ö.S., E.K., A.E., the acquisition of data. E.S.,Ö.S., Ş.K.Ş., the analysis, and interpretation of data and write the research paper. All authors approved the version to be published; and agree to be 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.

Ethics approval
All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.  Table 3. Psychometric Properties for Self-Rating Scales and Subscales