Japanese Journal of Clinical Oncology Advance Access originally published online on June 16, 2005
Japanese Journal of Clinical Oncology 2005 35(6):302-309; doi:10.1093/jjco/hyi097
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© 2005 Foundation for Promotion of Cancer Research
Psychiatric Disorders Following First Breast Cancer Recurrence: Prevalence, Associated Factors and Relationship to Quality of Life
1 Psychiatry Division, National Cancer Center Hospital East, Kashiwa, Chiba, 2 Psycho-Oncology Division, National Cancer Center Research Institute East, Kashiwa, Chiba, 3 Department of Psychiatry and Neurosciences, Graduate School of Biomedical Sciences, Hiroshima University, Hiroshima and 4 Department of Psychiatry, Nagoya City University Medical School, Nagoya, Japan
For reprints and all correspondence: Yosuke Uchitomi, Psycho-Oncology Division, National Cancer Center Research Institute East, 6-5-1 Kashiwanoha, Kashiwa 277-8577, Japan. E-mail: yuchitom{at}east.ncc.go.jp
Received March 4, 2005; accepted May 4, 2005
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Abstract |
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Objective: The purpose of this study was to investigate the prevalence of and factors associated with psychiatric disorders and the impact on quality of life (QOL) in patients with first breast cancer recurrence.
Methods: We analyzed the baseline data on 50 consecutively enrolled recurrent breast cancer patients, participating in a feasibility study of multifaceted psychosocial intervention. Psychiatric disorders, including major depressive disorder (MDD), dysthymic disorder, panic disorder, post-traumatic stress disorder (PTSD), generalized anxiety disorder and adjustment disorders (AD), were evaluated according to the Structured Clinical Interview for the DSM-III-R and IV. The patients' demographic data, biomedical factors, social support, mental adjustment to cancer, personality traits and QOL were also evaluated.
Results: Eleven (22%) met the DSM-III-R and IV criteria for MDD, PTSD or AD (MDD, 2%; PTSD, 2%; AD, 20%). Univariate analysis indicated that current doxorubicin/cyclophosphamide, presence of a confidant, past history of MDD, helplessness/hopelessness and neuroticism were significantly associated with psychiatric disorders. On multivariate logistic regression analysis, past history of MDD and helplessness/hopelessness were significant associated factors. Psychiatric disorders were significantly associated with lower functional scales (‘emotional functioning’, ‘body image’ and ‘future perspective’) and higher symptom scales (‘appetite loss’, ‘diarrhea’, ‘fatigue’ and ‘nausea–vomiting’) in QOL.
Conclusions: The result suggests that asking about history of depression and appropriate intervention, including psycho-education, are needed for patients with first breast cancer recurrence in order to detect and manage psychological distress. Although further studies are needed to clarify causal links between psychiatric disorders and QOL, patients' psychiatric disorders were associated with QOL.
Key Words: recurrent breast cancer • psychiatric disorders • associated factors • quality of life
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INTRODUCTION |
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Despite rapid advances in medicine and beneficial lifestyle changes, the incidences and mortality rates of gynecological carcinomas remain high worldwide (1). The incidence of breast cancer has been increasing remarkably in Japan (2,3). The age-standardized incidence rate of breast cancer was 43.6% (3), and is now the fifth leading cause of cancer-related deaths in Japanese women (4). About 30% of post-operative breast cancer will recur within 10 years. Even after passing the tenth post-operative year, cancer can still recur with a more fixed frequency. A number of treatment approaches have been used to manage recurrent breast cancer, but the gains in survival time have been modest and complete remission cannot be achieved in most cases (5).
Psychological distress is frequently observed in cancer patients during the clinical course of this disease. The prevalences of psychiatric disorders following a primary diagnosis of cancer were reported to range from 14 to 38% (6,7). Previous studies indicated that psychological distress is common in breast cancer patients and occurs throughout the course of the illness (8–10). In addition, it is known, in particular, that the recurrent phase of breast cancer is an extremely difficult time (11–14). Some reports have evaluated the psychological distress that follows recurrent breast cancer, and the prevalences of psychological distress including clinical anxiety and depression were higher (>40%) (15,16). Major depressive disorder, adjustment disorders and anxiety disorders appear to be common psychiatric disorders among recurrent breast cancer patients. Evaluation of psychiatric disorders is especially important in the advanced stages of disease, when the impending threats of pain, physical deterioration, uncertainty, and fear of death become burdensome. Also, various factors are considered to be associated with psychological distress (15–24), and these factors are intricately inter-related. However, no study has assessed a broad range of factors simultaneously, including biomedical and psychosocial variables that are potentially associated with psychological distress. Furthermore, psychological well-being is an essential element of quality of life (QOL) and also has an enormous impact on various dimensions of QOL in patients with a variety of cancers (25–29).
Therefore, we first evaluated the prevalences of psychiatric disorders, including major depressive disorder, dysthymic disorder, panic disorder, post-traumatic stress disorder (PTSD), generalized anxiety disorder and adjustment disorders, using a structured clinical interview, among breast cancer patients with a first recurrence. Secondly, we examined socio-demographic, biomedical and psychosocial factors associated with psychiatric morbidity. Thirdly, we investigated the impact of psychiatric disorders on QOL.
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METHODS |
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PARTICIPANTS
Women with recurrent breast cancer who participated in a feasibility study of multifaceted psychosocial intervention were studied (the results of the intervention study will be reported elsewhere). The subjects were consecutively recruited from out-patient populations of the Oncology-Hematology Division of the National Cancer Center Hospital East (NCCHE) in Japan during a 13 month period from January 2001 to January 2002. The eligibility criteria for the feasibility study of multifaceted psychosocial intervention were as follows: (i) histologically or cytologically documented breast cancer and a histologically, cytologically or clinically proven first recurrence of breast cancer; (ii) female, age 20 years or older; (iii) informed of recurrent diagnosis; (iv) disclosed their cancer recurrence from 1 to 6 months after detection of the recurrence; (v) an estimated life expectancy exceeding 6 months (as assessed by the primary physician); (vi) follow- up at the Oncology-Hematology Division of the NCCHE; and (vii) performance status (PS) from 0 (no symptoms) to 3 (>50% bedridden) according to the Eastern Cooperative Oncology Group PS. The exclusion criteria were: (i) cognitive impairment; (ii) too ill to participate; (iii) being treated for current psychiatric disorder; and (iv) unable to speak and understand Japanese. A previous report had shown that the prevalence of psychiatric disorders was very high (42%) in patients 3 months after their diagnoses of recurrent breast cancer (15) and at first we focused on patients 3 months after diagnoses for multifaceted psychological intervention. However, during a pilot study of intervention, we experienced various cases, for instance, a patient's first visit to our hospital was
4 months after recurrent diagnosis. Therefore, we chose to examine the patients from 1 to 6 months after their diagnoses of recurrence in order to intervene at 3 months. The reason for exclusion of patients with PS 4 is that we think interview for evaluation and questionnaires are too much of a burden on such patients and not possible to do in most cases.
PROCEDURE
This study was approved by the Institutional Review Board and the Ethics Committee of the National Cancer Center of Japan and was conducted in accordance with the Declaration of Helsinki. Written informed consent was obtained from each subject before the start of this study.
First, eligible patients received brief explanations of this study from their physician in the Oncology-Hematology Division, and then, if they consented to participate, were fully informed of the purpose of the study. Written consent was obtained from eligible patients, and an interview was then arranged (baseline). A psychiatric diagnosis and socio-demographic data were obtained in a structured interview by a trained psychiatrist (T.A.) or a research fellow (K.T.) who was trained for this study.
MEASURES
At baseline, the Structured Clinical Interview for DSM-III-R and IV (SCID) (30,31) was used during an interview to evaluate the patients for major depressive disorder, dysthymic disorder, panic disorder, PTSD, generalized anxiety disorder and adjustment disorders. A Japanese version of SCID is available for DSM-III-R but not DSM-IV. We therefore used the SCID for DSM-III-R to assess major depressive disorder, dysthymic disorder, panic disorder, generalized anxiety disorder and adjustment disorders. On the other hand, since no Structured Clinical Interview to assess PTSD was available, the authors translated the original SCID for DSM-IV for PTSD into Japanese and used it to assess PTSD in this study.
A structured interview was conducted to identify demographic factors, satisfaction with parenting and patients' use of confidants (presence and satisfaction) as indicators of social support. Patients' satisfaction with parenting scores ranged from 1 to 5: (1) ‘very dissatisfied’, (2) ‘fairly dissatisfied’, (3) ‘somewhat satisfied’, (4) ‘fairly satisfied’ and (5) ‘very satisfied’. In this interview, the patient was asked whether she had confided in someone since being diagnosed with cancer and, if she had a confidant, who that confidant was (32). The types of confidant included spouse, children, other family members (parents or siblings), friends, neighbors, colleagues, physician, nurse, priest or other. The patient was then asked how satisfied she was with interactions with these confidants. If the patient had not confided in anyone, she was asked about the degree of satisfaction with that state. Patients' responses ranged from 1 to 7: (1) ‘very dissatisfied’, (2) ‘fairly dissatisfied’, (3) ‘slightly dissatisfied’, (4) ‘somewhat satisfied’, (5) ‘slightly satisfied’, (6) ‘fairly satisfied’ and (7) ‘very satisfied’. Age, marital status and PS were determined at the time of the baseline survey. Medical data on sites of recurrence, the dates on which initial and recurrent diagnosis were confirmed, the disease-free interval, estrogen receptors, progesterone receptors, and current and past cancer treatments were obtained from the patients' medical charts.
Patients' responses to having cancer were assessed using the Mental Adjustment to Cancer (MAC) scale (33), a 40-item self-rating scale consisting of five subscales (fighting spirit, anxious preoccupation, fatalism, helplessness/hopelessness and avoidance). The validity and reliability of the Japanese version of the MAC scale have been confirmed (34). Each item was rated on a scale of 1–4, ranging from ‘definitely does not apply to me’ to ‘definitely applies to me’. Helplessness/hopelessness is characterized by a tendency to feel hopeless and helpless about oneself and the future because of having cancer and the adoption of a wholly pessimistic attitude, whereas fighting spirit is characterized by a tendency to confront and deal with the illness and by adoption of an optimistic attitude.
Patients' personality traits were assessed using the Eysenck Personality Questionnaire-Revised (EPQR) (35), a 48-item self-rating scale consisting of four subscales (psychoticism, extraversion, neuroticism and lie). The validity and reliability of the Japanese version of the EPQR have been confirmed (36). Extraversion is a reflection of sociability and liveliness, whereas neuroticism reflects emotional instability and anxiousness.
Patients' QOL was assessed using the European Organization for the Research and Treatment of Cancer (EORTC) QLQ-C30 and QLQ-BR23. The QLQ-C30 is a 30-item self-report questionnaire covering functional and symptom-related aspects of QOL for cancer patients (37). It is a multi-dimensional questionnaire consisting of nine scales: five are functional scales (physical, role, cognitive, emotional and social), three are symptom scales (fatigue, pain and nausea, and vomiting) and one is a global health status and QOL scale. There are also six single item measures (dyspnea, insomnia, appetite loss, constipation, diarrhea and financial difficulties). The QLQ-C30, also known as the core questionnaire, may be used for all cancer patients, but there are supplementary questionnaires (modules) specific to the cancer being studied. The QLQ-BR23 is the breast cancer module, and consists of 23 questions assessing disease symptoms, adverse treatment events, body image, sexuality and future perspective (38). A high score for a functional scale represents a high level of functioning, and a high score for global health status and quality of life represents a high QOL. On the other hand, a high score for a symptom scale or item represents a high level of symptomatology and problems. The validity and reliability of the Japanese version of the EORTC QLQ-C30 and QLQ-BR23 have been confirmed (39,40).
STATISTICAL ANALYSIS
The presence or absence of psychiatric disorders was entered into the analysis as a dependent variable. Associated factors were assessed by univariate and multivariate analyses. Socio-demographic, biomedical and psychosocial factors were compared between two groups using the 
2 test, Fisher's exact test and the Mann–Whitney non-parametric test, respectively. Socio-demographic, biomedical and psychosocial variables that significantly correlated with a dependent variable in the univariate analyses (P < 0.05) were entered into the logistic regression analysis. We compared scale scores of the EORTC QLQ-C30 and QLQ-BR23 between two groups using the Mann–Whitney non-parametric test.
Differences with a P-value of <0.05 were considered significant. All P-values were two-sided. For all data analyses, we used SPSS Version 12.0 J for Windows statistical software (SPSS Japan Institute Inc., Tokyo, Japan, 2003).
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RESULTS |
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PATIENT CHARACTERISTICS
There were 72 women with recurrent breast cancer during the study entry period, but 13 were ineligible (currently being treated for psychiatric disorders, n = 4; no follow-up in the NCCHE, n = 4; too ill, n = 2; others, n = 3). Of the 59 eligible patients, 50 agreed to participate (response rate; 85%). Nine patients refused. The mean age of the participants was 53 years (SD, 10; range, 32–72; median, 54). Eighty percent had >12 years of formal education. Eighty-four percent were married, and 86% had children. Ninety-three percent were satisfied with parenting their children. Ninety-six percent lived with their families. Few patients (4%) reported that they had no confidants, and 64% were satisfied with their confidants.
PS was grade 0 in 40 patients (80%), grade 1 in eight (16%), and grade 2 in two (4%). Ninety-eight percent had distant metastases. The sites of cancer recurrence were bone (n = 18; 36%), lymph nodes (n = 15; 30%), lung (n = 13; 26%), liver (n = 10; 20%) and skin (n = 8; 16%). Sixty-two percent were undergoing chemotherapy (doxorubicin/cyclophosphamide 24%, docetaxel 20%, paclitaxel 2%), 48% hormone therapy and 2% radiation therapy. Forty-eight percent had disease-free intervals <24 months. Seven patients (14%) had a history of major depressive disorder. Four patients had experienced a major depressive episode after the onset of breast cancer (immediately after diagnosis of cancer, two; after surgery, two).
PREVALENCES of PSYCHIATRIC DISORDERS
Of the 50 subjects, 11 (22%) met the DSM-III-R and IV criteria for major depressive disorder, adjustment disorders or PTSD. Major depressive disorder was seen in one (2%), adjustment disorders in 10 (20%) (four with depressive mood, one with anxious mood and five with both depressive and anxious mood) and PTSD in one (2%). One patient had both PTSD and adjustment disorders. None had dysthymic disorder, panic disorder or generalized anxiety disorder.
FACTORS ASSOCIATED WITH PSYCHIATRIC DISORDERS
We compared socio-demographic, medical and psychological factors between patients with and without psychiatric disorders (Table 1). The sites of cancer recurrence, disease-free interval, education and marital status were not associated with having a major depressive disorder, adjustment disorders or PTSD. The factors that were significantly associated with the presence of psychiatric disorders were: current treatment with doxorubicin/cyclophosphamide (P = 0.014); presence of confidants (P = 0.045); helplessness/hopelessness (P = 0.003); neuroticism (P = 0.023); and past history of major depressive disorder (P = 0.004).
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Using these significant correlated factors in univariate analysis, we conducted a logistic regression analysis to identify independent risk factors for psychiatric disorders (Table 2). The results revealed past history of major depressive disorder (P = 0.027) and helplessness/hopelessness (P = 0.037) to be significantly associated with a diagnosis of major depressive disorder, adjustment disorders or PTSD. Five out of 11 patients with psychiatric disorders (45%) had a past history of major depressive disorder. Three patients experienced a major depressive episode after the onset of breast cancer (immediately after diagnosis of cancer, one; after surgery, two). Current treatment with doxorubicin/cyclophosphamide showed borderline significance (P = 0.092).
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ASSOCIATION BETWEEN PSYCHIATRIC DISORDERS AND QUALITY OF LIFE
The patients' psychiatric disorders were significantly associated with lower functional scales (‘emotional functioning’, ‘body image’ and ‘future perspective’) and higher symptom scales (‘appetite loss’, ‘diarrhea’, ‘fatigue’ and ‘nausea–vomiting’) in QOL (Table 3), while ‘global health status’, other functional scales and other symptom scales were not.
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DISCUSSION |
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This is the first study to clarify the prevalences of a wide range of psychiatric disorders including major depressive disorder, dysthymic disorder, panic disorder, generalized anxiety disorder, PTSD and adjustment disorders, and associated factors, as well as the impact of psychiatric disorders on QOL among patients with a first recurrence of breast cancer.
The present investigation demonstrated the prevalence rate of psychiatric disorders to be 22% in recurrent breast cancer patients. This rate is similar to the DSM-III-, DSM-III-R- or DSM-IV-assessed rate observed following primary diagnosis of cancer (14–38%) (6,7). However, this prevalence is lower than that in our previous report on recurrent breast cancer (42%) (15). The response rate for our previous study was 98%, in contrast to 85% for the current study. If patients who refused to participate had psychiatric disorders, the prevalence might be similar. It seems that the discrepancy between these results is not large.
Another difference was that the sample group for the current study participated in a feasibility study of multifaceted psychosocial intervention. We evaluated psychiatric disorders somewhat broadly, not only major depressive disorder and adjustment disorders, but also dysthymic disorder, panic disorder, PTSD and generalized anxiety disorder. It might, however, be possible to underestimate psychiatric disorders because of the low participation rate. The prevalence of major depressive disorder (2%) was lower than those in the previous reports on advanced cancer patients (5–26%) (41). Small sample size or the refusal rate might have contributed to the low prevalence. Furthermore, there is a generally lower prevalence of major depression in Asian countries, among both patients with cancer and the general population, as compared with Western countries, possibly because of cross-cultural differences (e.g. social stigma, cultural reluctance to acknowledge mental symptoms and low divorce rate) (42). This difference might be responsible for the inconsistent findings. The results also suggest that few of our subjects experienced PTSD. Since several studies using psychiatric interviews to assess PTSD in breast cancer patients have found low prevalences of PTSD, ranging from 3 to 19% (10,43–48), PTSD morbidity seems to be rare in breast cancer patients with various disease stages. However, no study has assessed PTSD in recurrent breast cancer patients. In terminally ill cancer patients, there was no PTSD as evaluated by means of the DSM-IV (49). Even in recurrent cancer patients, cancer-related experiences themselves may not be common traumatic events that result in a clinical diagnosis of PTSD.
The associations of psychiatric disorders with past history of major depressive disorder and helplessness/hopelessness remained significant in multivariate analysis. Studies on factors associated with psychological distress in various cancers have identified physical variables, such as pain, fatigue, other symptom burdens and poor PS, as biomedical factors (17–20), whereas other studies have indicated socio-demographic and psychosocial variables, such as younger age (17,21,22) and social support, including marital status (23,24), to be important. Regarding recurrent breast cancer, previous studies indicated that factors associated with psychological distress included previous psychiatric illness, trait neuroticism and a disease-free interval of <24 months (15,16). The association of past history of major depressive disorder with psychiatric disorders is consistent with previous studies of breast cancer patients (8,16,50). Those who had a major depressive episode after the onset of breast cancer are considered to have a higher risk of repeated psychiatric disorders. This result suggests that screening and intervention for psychological distress are needed after diagnosis, surgery and recurrence of breast cancer in order to detect clinical psychological distress earlier, to manage it appropriately and to prevent recurrence of psychiatric disorders. Significant associations between higher scores of helplessness/hopelessness and psychological distress were detected in several studies of subjects with various cancers, at different clinical stages (51–53). The findings suggest that past history of major depressive disorder and helplessness/hopelessness are both independently associated with psychiatric disorders experienced by recurrent breast cancer patients. It appears to be important to evaluate past history of major depressive disorder as an approach to improving mental adjustment to cancer after diagnosis of this disease.
A previous report indicated that a disease-free interval shorter than 24 months significantly predicted psychological distress following a first recurrence of breast cancer (15). On the other hand, our current results are not consistent with this view. The previous study investigated 55 patients, the current study 50 patients. As the sample sizes of both studies were small, further investigations involving larger samples are needed to clarify the association between psychiatric disorders following breast cancer recurrence and a shorter disease-free interval. In multivariate analysis, current treatment with doxorubicin/cyclophosphamide showed borderline significance. Adverse effects during chemotherapy are known to be related to increased emotional distress and to disrupt the activities of daily living (54). Each chemotherapy regimen influences patients differently. Love et al. reported treatment difficulty to be significantly different across regimen groupings for breast cancer or malignant lymphoma (54). The CAF (cyclophosphamide, doxorubicin and 5-fluorouracil) regimens were consistently associated with the highest levels of difficulty, and patients on the CAF regimens also had higher levels of disruption, in both their social lives and work. Kramer et al. reported that doxorubicin was associated with a significantly greater burden of disease and treatment than paclitaxel for advanced breast cancer (55). This current result suggests that oncologists should pay careful attention to a patient's mental status during chemotherapy, especially with doxorubicin/cyclophosphamide.
The present study found that patients with psychiatric disorders experienced declines in several domains of QOL as compared with patients without psychiatric disorders, as has been observed by others (25–29). In previous reports, depression and anxiety were assessed by the Hospital Anxiety and Depression Scale, the Centre for Epidemiologic Studies Depression Scale, the Beck Depression Inventory or the State-Trait Anxiety Inventory (26–29). Stark et al. (25) assessed anxiety disorders using ICD-10 psychiatric diagnoses, but not other psychiatric disorders. To our knowledge, this is the first study to clarify the association between psychiatric disorders assessed by means of the SCID and QOL among recurrent breast cancer patients. Also, no study has been conducted to examine this association among any cancer patients in Japan. Psychiatric disorders were associated with lower functional scales (‘emotional functioning’, ‘body image’ and ‘future perspective’) and higher symptom scales (‘appetite loss’, ‘diarrhea’, ‘fatigue’ and ‘nausea and vomiting’) in QOL. Psychiatric disorders might be responsible for lower ‘emotional functioning’ and lower ‘future perspective’. Surgical treatments for breast cancer often lead to body image problems (56). Bull et al. reported that women with recurrent breast cancer had experienced moderate problems associated with body image, but there was no change prior to recurrence, immediately after recurrence and 6 months after recurrence (57). Our results suggest that patients with psychiatric disorders might experience more severe body image problems than those without such disorders. Higher symptom scales, especially ‘appetite loss’ and ‘fatigue’, could account for a portion of psychological symptoms, or patients with psychiatric disorders might be susceptible to experiencing the symptom burden. These results suggest that it is important to manage stressful physical conditions and to evaluate psychiatric disorders simultaneously. As adverse effects during chemotherapy are known to be related to increased emotional distress and to disrupt the activities of daily living (54), further studies are needed to clarify whether these disorders impair psychosocial and physical aspects of QOL.
There were several limitations to this study. First, we used baseline data from a feasibility study of multifaceted psychosocial intervention for recurrent breast cancer. Furthermore, the sample size was small. Thirteen of 72 patients were ineligible (treating current psychiatric disorders, n = 4; no follow-up in the NCCHE, n = 4; too ill, n = 2; others, n = 3). Ineligible patients might have had psychiatric disorders. Despite this being a prevalence study, patients who were treated for current psychiatric disorders were excluded. These limitations may have resulted in underestimation of the prevalence of psychiatric disorders and distortion of the associated factors. Secondly, since the study was conducted only in one institution, a teaching cancer center hospital, institution bias may be another problem. Thirdly, this study was cross-sectional, a design allowing interpretation of potential causal associations between psychiatric disorders and QOL. Because of these limitations, further studies are needed to clarify whether the psychiatric disorders described herein can impair psychosocial and physical aspects of QOL.
Despite these limitations, the findings of this study indicate that past history of major depressive disorder and helplessness/hopelessness are significantly associated with a diagnosis of major depressive disorder, adjustment disorders or PTSD, and that those who had a major depressive episode after the onset of breast cancer are at higher risk of repeated psychiatric disorders. As there have been some randomized clinical trials demonstrating psychological treatment for metastatic breast cancer to be useful for improving psychological outcomes (58), the present results suggest that screening and intervention for psychological distress should be recommended after diagnosis, surgery, and recurrence of breast cancer. In addition, certain approaches, such as psycho-educational intervention to improve mental adjustment to cancer, are also needed. Detection and treatment of anxiety and depression should be achieved to facilitate relief of physical symptoms and to improve QOL.
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Acknowledgments |
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We are grateful to the physicians of the Oncology-Hematology Division of the National Cancer Center Hospital East (Drs H. Minami, K. Ito, M. Tahara, H. Mukai and M. Nakata) for enrolling their patients in this study, and Dr S. Suzuki, Ms Y. Kojima, RN, Ms R. Katayama and Ms Y. Sugihara, BA, of the Psycho-Oncology Division, National Cancer Research Institute East, for their research assistance. We would also like to thank M. Iwasaki MD, PhD, Epidemiology and Prevention Division, Research Center for Cancer Prevention and Screening, National Cancer Center, for his helpful statistical advice. K.T. is an Awardee of Research Resident Fellowships from the Foundation for Promotion of Cancer Research in Japan. This study was supported in part by a Grant-in-Aid for Medical Frontier Strategy Research, a Grant-in-Aid for Cancer Research, and the Second-Term Comprehensive 10-Year Strategy for Cancer Control and Research of the Japanese Ministry of Labor, Health and Welfare.
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References |
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