Anxiety in disease-free breast cancer patients might be alleviated by provision of psychological support, not of information

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1 Japanese Journal of Clinical Oncology, 2015, 45(10) doi: /jjco/hyv112 Advance Access Publication Date: 16 July 2015 Original Article Original Article Anxiety in disease-free breast cancer patients might be alleviated by provision of psychological support, not of information Tatsuo Akechi 1,2, *, Kanae Momino 3, Mitsunori Miyashita 4, Nobuhiro Sakamoto 2,5, Hiroko Yamashita 6,7, and Tatsuya Toyama 6 1 Department of Psychiatry and Cognitive-Behavioral Medicine, Nagoya City University Graduate School of Medical Sciences, Nagoya, Aichi, 2 Division of Palliative Care and Psycho-oncology, Nagoya City University Hospital, Nagoya, Aichi, 3 Nagoya City University Graduate School of Nursing, Nagoya, Aichi, Japan, 4 Department of Palliative Nursing, Health Sciences, Tohoku University Graduate School of Medicine, Sendai, Japan, 5 Department of Gastroenterological Surgery, Nagoya City University Graduate School of Medical Sciences, Nagoya, Aichi, 6 Department of Oncology, Immunology and Surgery, Nagoya City University Graduate School of Medical Sciences, Nagoya, Aichi, Japan, and 7 Breast Surgery, Hokkaido University Hospital, Sapporo, Japan *For reprints and all correspondence: Tatsuo Akechi, Department of Psychiatry and Cognitive-Behavioral Medicine, Nagoya City University Graduate School of Medical Sciences, Mizuho-cho, Mizuho-ku, Nagoya, Aichi , Japan. takechi@med.nagoya-cu.ac.jp Received 24 April 2015; Accepted 29 June 2015 Abstract Objective: This study investigates the prevalence of clinical anxiety, the possible impact of patients anxiety on quality of life and the association between their anxiety levels and patients perceived needs. Methods: Randomly selected disease-free patients with breast cancer who survived >2 years were invited to participate in the study. The participants were asked to complete the Hospital Anxiety and Depression Scale, the European Organization for Research and Treatment of Cancer QLQ-C 30 and the Short-form Supportive Care Needs Survey questionnaire, which covers five domains of need (health system and information, psychological, physical, care and support and sexuality needs). Results: Complete data were available for 146 of the patients, and 14% of them suffered from clinical anxiety. Anxiety score had a statistically significant correlation with all domains of quality-of-life measures. The only perceived need that was significantly associated with anxiety was the psychological domain. Conclusions: Not negligible patients may suffer from clinical anxiety >2 years after their initial cancer diagnoses. Anxiety can impact on patients quality of life, and unmet psychological needs are expected to increase anxiety levels. Management of anxiety could be one of the key components to improving the quality of life for breast cancer survivors and that reducing their unmet psychological needs may contribute to alleviating anxiety. Key words: anxiety, survivors, need, quality of life, supportive care The Author Published by Oxford University Press. All rights reserved. For Permissions, please journals.permissions@oup.com 929

2 930 Anxiety in disease-free breast cancer survivors Introduction Breast cancer is one of the most common forms of cancer affecting women worldwide. In Japan, it is the most common form of cancer afflicting women, and its prevalence is increasing every year. In Japan, latest estimates state that approximately additional women are diagnosed with breast cancer every year. Advances in early detection and individualized medical treatment have improved the survival rate of breast cancer patients, enabling them to live for longer periods of time. The current 5-year and 10-year survival rates for patients with breast cancer are approximately 90 and 80% respectively, which indicates that the number of breast cancer survivors continues to increase (1). Despite patients with breast cancer having a better prognosis on average than many other types of cancer patients, it is suggested that many breast cancer survivors can suffer from anxiety and uncertainty (2,3), especially when there is a recurrence of cancer (4). A recent meta-analytical study that examined depression and anxiety in longterm cancer survivors (i.e. patients diagnosed with cancer at least 2 years previously) found that the prevalence of anxiety among such patients was 17.9%, which was significantly higher than that in the healthy control group (5). However, the prevalence of depression for the cancer survivors was comparable with that of the controls (5). On the other hand, while many studies have investigated psychosocial issues encountered by patients with breast cancer (6 9), not many have focused on prevalence of anxiety and its associated factors among breast cancer survivors (2,10,11). Previous Australian and UK studies demonstrate that the prevalence of the cases of anxiety assessed by Hospital Anxiety and Depression Scale among breast cancer survivors 2 10 years and at least 2 years after diagnosis are 18 and 33%, respectively (2,12). UK studies indicates that the point prevalence of depression and/or anxiety among breast cancer survivors 2 5 years after diagnosis is 15 25% and that younger age, previous psychological treatment, lack of social support and stressful non-cancer life experiences are associated with longer term psychological morbidities (13). A Chinese study indicates that poor psychological adjustment during the first year diagnosis can predict higher anxiety 6 years later (14). An American study shows that 8% of the breast cancer survivors who were no longer receiving adjuvant chemotherapy are receiving benzodiazepines (15). Thus some studies suggest that not negligible proportion of breast cancer survivors suffer from anxiety even 2 years or more after cancer diagnosis, however, for the development of novel and effective interventions for reducing anxiety levels in patients with breast cancer, more information is needed on the factors that influence it. In addition, there are also a few data on the potential impact of clinical anxiety on quality of life (QOL) among breast cancer survivors and these studies suggest significant association between anxiety among breast cancer survivors and patients QOL (16). To this end, this study investigates the prevalence of clinical anxiety, the relationship between a patient s anxiety level and QOL and that between a patient s anxiety level and his or her underlying perceived needs among long-term disease-free breast cancer patients. Patient needs in terms of underlying factors were included in this study because directly asking patients about them provided a clearer picture of what resources they think they need, even though patients problems and symptoms do not necessarily reflect their actual need for help (17,18). Namely, if we understand the actual domains of the patients needs (e.g. information needs) that are significantly associated with anxiety, we can develop novel intervention program (e.g. information provision or educational intervention) that can potentially contribute to ameliorate patients anxiety. Patients and methods Participants This study was conducted using data from previous study published in 2011 (8). Eligibility criteria for inclusion in that study stated that patients must (i) have a diagnosis of breast cancer, (ii) be at least 20 years of age, (iii) be aware of his or her cancer diagnosis, (iv) have no evidence of recurrence or metastasis and (iv) possess a general condition sufficient to allow the completion of the survey questionnaire [0 3on the Eastern Cooperative Oncology Group (ECOG) performance status]. Exclusion criteria included patients with (i) severe mental or cognitive disorders or (ii) an inability to understand the Japanese language. The study participants were female patients with breast cancer who had visited the outpatient clinic for Oncology, Immunology and Surgery at the Nagoya City University Hospital between February 2006 and February Potential participants were chosen at random using a visiting list and random number table. The current study subjects were extracted from this previous study participants if the patients were recurrence-free female breast cancer survivors who survived >2 years. We selected the patients who survived >2 years according to the previous studies including meta-analysis (2,5). The study was approved by the Institutional Review Board and Ethics Committee of the Nagoya City University Graduate School of Medical Sciences in Japan and was conducted in accordance with the principles described in the Helsinki Declaration. Written consent was obtained from each patient after they received a thorough explanation of the purpose and method of the study. Procedure After obtaining the informed consent of the patients, they were asked to complete the self-administered questionnaires (described below) at home and return them the following day. If any of the questions were answered inadequately, necessary clarification was sought via telephone interviews. Anxiety and psychological distress: Hospital Anxiety and Depression Scale The Hospital Anxiety and Depression Scale (HADS) has been developed for use in physically ill patients and does not contain any questions that ask about physical symptoms. The HADS is a self-reported questionnaire consisting of 14 items, with both an anxiety and a depression subscale (0 21 points each), and the total score can range from 0 to 42. A higher score indicates more severe depression and anxiety (19). The Japanese version of the HADS was found to have validity when used with cancer populations (20). The optimal cut-off point of anxiety subscale when screening for clinical anxiety suggesting the presence of adjustment disorders and major depressive disorders was 7/8 (20). Before filling out the Japanese version of the HADS, patients were asked to rate how they felt emotionally during the course of the previous week using a four-point Likert scale. QOL: EORTC QLQ-C 30 Patient QOL was assessed using EORTC QLQ-C30 (21), which is a 30-item, self-report questionnaire that collects information about functional aspects (e.g. global health status, physical functioning, role functioning, emotional functioning, cognitive functioning and social functioning) and symptom-related aspects (e.g. fatigue, nausea and vomiting, pain, dyspnea, insomnia, appetite loss, constipation, diarrhea and financial difficulties) of QOL in cancer patients (21). The validity and reliability of the Japanese version of EORTC

3 Jpn J Clin Oncol, 2015, Vol. 45, No QLQ-C30 were established in previous studies (22): high functional score represents high QOL, and high symptom score indicates severe physical symptoms. Patients perceived needs: the short-form supportive care needs survey questionnaire The short-form supportive care needs survey questionnaire (SCNS-SF34) is a self-administered instrument for assessing the perceived needs of cancer patients (23), consisting of 34 items covering five different domains of needs: psychological (10 items), healthcare system and information (11 items), physical and daily living (5 items), patient care and support (5 items) and sexuality (3 items). The patients were asked to indicate the amount of help they needed over the last month in relation to their cancer treatments using the following five response options: 1 [No Need (Not applicable)], 2 [No Need (Satisfied)], 3 [Low Need], 4 [Moderate Need] and 5 [High Need]. Subscale scores were obtained by adding up the scores for the individual items within each subscale. In addition, the total score on the entire questionnaire was obtained by adding all the subscale scores together (range, ). A higher score indicated higher perceived need. The scale can also be used to obtain information on the presence, the absence and the number of perceived unmet needs (a rating of 3 or higher was considered an unmet need), depending on the researcher s clinical question. The validity and reliability of the Japanese version of the SCNS-SF34 was established in previous studies (24). Focusing on patient needs in a healthcare setting offered a number of advantages. For patients, perceived needs are important because they reflect their actual need for help, while their problems and symptoms may not. Therefore, we decided to assess the patients needs that they believe should have been provided on the basis of their preferences. Sociodemographic and biomedical factors An ad hoc self-administered questionnaire was used to collect sociodemographic information about the patients, such as marital status, education levels and employment status. Their performance statuses, as defined by the European Cooperative Oncology Group (ECOG), were measured by the attending physicians. All other medical information, such as duration since diagnosis, clinical stage and type anticancer treatment, was obtained from medical records. Statistical analyses First, Pearson s correlation analysis was conducted to measure the strength of the relationship between anxiety and QOL. Second, to investigate the strength of association between anxiety and patients underlying perceived needs, multiple regression analysis was conducted. In this type of analysis, anxiety scores were treated as the dependent variable, and scores for all five domains of the patients perceived needs were considered independent variables. Age, marital status, education, employment status, period from cancer diagnosis and physical functioning were also considered independent variables as covariates because these are potentially confounding factors (8,25 30). A P value of <0.05 was regarded as being statistically significant, and all reported P values were two-tailed. All statistical procedures were conducted using IBM SPSS Statistics version 19 software for Windows (SPSS Inc., 2010). Results Patient characteristics Three hundred and forty-six potential participants whose cancers were either recurrent or metastatic free were initially identified from the previous study database (8). Among them, 200 patients were excluded because 192 of them were cancer free within 2 years of being diagnosed, 7 refused to participate and 1 was excluded due to an incomplete medical history. Both the sociodemographic and clinical characteristics of the remaining 146 patients are presented in Table 1. The mean (±SD) and median ages of the study population were both 57 years (±11). Most of the patients did not have impairments of physical functioning. The mean (±SD) and median duration of days since diagnosis were 1569 (±786) and 1321 (range: ) days, respectively. During the course of this study, 75 patients (51%) were still undergoing hormonal therapy. The HADS scores revealed that 14% of the subjects suffered from clinical anxiety (HADS anxiety 8). Table 1. Characteristics of the study participants (n = 146) Characteristics N % Age (in years) mean: 57 (SD = 11), median: 57 (range, 27 87) Marital status Married Education >12 years Employment status Full-time /part-time Clinical stage I II III 6 4 Performance status Duration since diagnosis (days) mean: 1569 (SD = 786), median: 1321 (range, ) Past anticancer treatment a Surgery Chemotherapy Trastuzumab 1 1 Hormonal therapy Radiation therapy HADS score b a Multiple choice. b HADS, Hospital Anxiety and Depression Scale.

4 932 Anxiety in disease-free breast cancer survivors Anxiety level was significantly associated with all quality-of-life measures both including functional aspects (global health status, physical functioning, role functioning, emotional functioning, cognitive functioning, social functioning and financial difficulties) and symptom-related aspects (fatigue, nausea/vomiting, pain, dyspnea, insomnia, appetite loss, constipation and diarrhea) (see Table 2). With regard to association between perceived needs and anxiety levels, only the psychological needs domain was significantly associated with anxiety level while health system and information, physical, care and support and sexuality needs were not (see Table 3). Discussion The most significant findings of the study were that, anxiety level was significantly associated with all domains of QOL, and unmet psychological needs may influence anxiety levels among disease-free breast cancer patients. With regard to the psychological distress scores, the prevalence of clinical anxiety suggest that not negligible proportion of the breast cancer survivors may have suffered from clinical anxiety more than 2 years after their initial cancer diagnoses although the prevalence Table 2. Associations between anxiety a and QOL (n = 146) b Association between anxiety and QOL Correlation coefficients P values Global health status 0.58 <0.001 Physical functioning 0.36 <0.001 Role functioning 0.41 <0.001 Emotional functioning 0.67 <0.001 Cognitive functioning 0.43 <0.001 Social functioning 0.40 <0.001 Financial difficulties 0.39 <0.001 Symptom-related aspects Fatigue 0.56 <0.001 Nausea/vomiting 0.34 <0.001 Pain 0.44 <0.001 Dyspnea 0.42 <0.001 Insomnia 0.33 <0.001 Appetite loss 0.46 <0.001 Constipation Diarrhea a Assessed by Hospital Anxiety and Depression Scale. b Assessed by EORTC QLQ-C30. Table 3. Patients supportive care needs associated with anxiety-multiple regression analysis (n = 146) a Patients perceived needs b Coefficient (B) Standardized coefficient (β) Psychological <0.001 Health system and information Physical and daily living Patient care and support Sexuality R 2 = 0.52 a Adjusted for age, marital status, education, employment status, period from cancer diagnosis and physical functioning. b Assessed by the Short-form Supportive Care Needs Survey questionnaire. t P of clinical anxiety may have been lower than the rate of recurrent breast cancer and other types of advanced cancer (26,28,31). These findings suggest that some of the breast cancer survivors may need more psychological support from oncology staff than was previously provided, and that psychosocial interventions that focus specifically on reducing anxiety levels may prove helpful. For breast cancer survivors, a significant relationship between anxiety levels and QOL indicated that anxiety was one of the key factors in determining a QOL. Therefore, finding ways to reduce anxiety levels of patients may be essential to improving their QOL. While previous studies have indicated that the type of medical condition, the amount of social support and the current income level were strong positive predictors of QOL (32), the findings in this study suggest that reducing a patient s anxiety level may also be a relevant factor for maintaining QOL. For the symptom-related aspects of QOL, the strongest positive correlation (0.56) was observed between fatigue and anxiety level. This finding was in line with the results in previous systematic reviews that suggested that breast cancer survivors still suffered from fatigue after active anticancer treatment (33). Based on this finding and the fact that fatigue is one of the relevant clinical symptoms required to meet the diagnostic criteria of generalized anxiety disorder (34), anxiety may partly influence how much fatigue breast cancer survivors experience. Therefore, these findings suggest that interventions designed to reduce breast cancer patients anxiety levels may also help reduce the amount of fatigue they feel. The significant association that was found between patients perceived needs and anxiety levels indicate that there are many different strategies that could be used to reduce patients anxiety levels. The current study also demonstrated that only unmet psychological needs (and none of the other four domains) were significantly associated with anxiety. This may simply imply that treatment for anxiety by itself, rather than the provision of information or treatment for the physical condition, could be the most important component for reducing patients anxiety depending on the patients needs. In addition, previous studies have consistently indicated that patients prefer psychotherapeutic intervention to pharmacological treatments for ameliorating psychological distress (35,36). Therefore, it may be beneficial for breast cancer patients if a new psychological intervention program to treat their anxiety was developed. It should be noted, however, that survivors anxiety is not always pathological and often reflects legitimate concerns, including fear of recurrence for patients in the advanced cancer population (37). Since the results from our previous study indicated that breast cancer survivors problem-solving abilities were significantly associated with their fear of recurrence and anxiety levels (38), psychological intervention programs that also help improve these abilities could help reduce breast cancer survivors anxiety. The present study had several limitations. First, the investigation was cross-sectional in design, which eliminated any chance for conclusions to be drawn with regard to causality between patients anxiety levels, QOL and needs over time. Second, only general QOL measures were included, so they may not have provided the clearest picture of survivors QOL (39). Third, because supportive care needs could have been influenced by the patients cultural backgrounds and their respective countries medical systems, the results may not be applicable to other patient populations. Finally, since the present study was only conducted at one institution, an institutional bias may have tainted the results. In conclusion, the results of this study suggested that patients anxiety levels were significantly associated with all five domains of QOL measured in this study. They also suggested that patients unmet psychological needs may contribute to anxiety levels among disease-free breast cancer patients. These two findings suggest that effective

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