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Major Depression, Adjustment Disorders, and Post-Traumatic Stress Disorder in Terminally Ill Cancer Patients: Associated and Predictive Factors

From the Psycho-Oncology Division, National Cancer Center Research Institute East, Chiba; Psychiatry Division and Palliative Care Unit, National Cancer Center Hospital East, Tokyo, Japan.

Address reprint requests to Yosuke Uchitomi, MD, PhD, 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

	ABSTRACT

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... REFERENCES

 
PURPOSE: Few studies have been conducted to elucidate the psychological distress of terminally ill cancer patients. This study attempted to determine the prevalence of adjustment disorders (AD), major depression (MD), and post-traumatic stress disorder (PTSD) among terminally ill cancer patients, to identify factors that contribute to them, and to determine how they change longitudinally.

PATIENTS AND METHODS: Consecutive terminally ill cancer patients were recruited. Patients were assessed for psychiatric disorders by structured clinical interview twice: once at the time of their registration with a palliative care unit (baseline), and again at the time of their palliative care unit admission (follow-up). Possible contributed biomedical and psychosocial factors were evaluated.

RESULTS: The proportions of patients diagnosed with AD, MD, and PTSD at baseline (n = 209) were 16.3%, 6.7%, and 0% respectively, whereas at follow-up (n = 85), 10.6% were diagnosed with AD and 11.8% with MD. Lower performance status, concern about being a burden to others, and lower satisfaction with social support were significantly associated with AD/MD at baseline. There were changes in the diagnosis of AD and MD in 30.6% of the patients. Only the Hospital Anxiety and Depression Scale at the baseline was significantly predictive of AD/MD at follow-up.

CONCLUSION: The factors underlying psychological distress are multifactorial. Early intervention to treat subclinical anxiety and depression may prevent subsequent psychological distress.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... REFERENCES

 
Because cancer is a life-threatening disease, its psychological impact on patients has been an important aspect of clinical oncology. Derogatis et al¹ found that almost half of cancer patients had been diagnosed with a psychiatric disorder, and that most of them had an adjustment disorder and/or major depression. Other studies have consistently indicated that adjustment disorders and major depression are common psychiatric disorders among cancer patients^2-4 and are more common in patients with advanced cancer and/or in cancer patients who are terminally ill.^4,5 Several studies investigating the prevalence of these psychiatric disorders in terminally ill cancer patients by rigorous diagnostic methods (eg, structured clinical interview) have revealed rates of adjustment disorders of 9% to 35% and rates of major depression of 8% to 26%.^2,3,6-14 Because a diagnosis of life-threatening illness now meets the traumatic stressor exposure criteria of the Diagnostic and Statistical Manual of Mental Disorders (DSM-IV) for post-traumatic stress disorder (PTSD),¹⁵ several studies have focused on PTSD or post-traumatic stress symptoms in cancer patients.^16,17 Although the results have demonstrated that 3% to 35% of cancer patients experience full-syndrome PTSD or post-traumatic stress symptoms in this population,^17-24 most studies have focused on early- and mixed-stage cancer patients, and to the best of our knowledge only two studies have investigated post-traumatic stress symptoms in patients with advanced cancer.^25,26 Based on the results of a self-report questionnaire, those studies suggested that clinically significant levels of intrusion and avoidance symptoms related to their cancer were experienced by 34% to 43% and 28% to 80% of the subjects, respectively.^25,26 However, the fact that a precise method of assessment, such as the structured diagnostic interview, was not used in those studies, the value of their findings was limited.

Several studies have indicated that psychological distress can have a serious negative impact on patients with advanced cancer and/or terminally ill cancer patients, including reducing their quality of life,²⁷ causing severe suffering²⁸ and a desire for early death, requests for physician-assisted suicide and/or euthanasia,^6,9,13,29 suicide,³⁰ as well as psychological distress in family members.³¹ Nevertheless, the psychological distress experienced by cancer patients is often under-recognized by the medical staff in clinical oncology settings.^32,33

On the other hand, there has been very little information as to why some terminally ill cancer patients suffer such distress and others do not. Although some investigators have suggested several possible risk factors for psychological distress in terminally ill cancer patients, ie, age (younger), sex (female), physical symptoms (eg, pain), physical functioning, cancer site (pancreatic cancer), cancer therapy (eg, chemotherapy, radiotherapy), brain metastasis, hypercalcemia, use of steroids, several types of concerns (existential concerns), past history of major depression, and social support,^34-36 surprisingly, no studies have actually provided evidence in support of them. Although aggressive prevention and management of psychological distress is a critical aspect of their care, hardly any is available concerning knowledge of factors associated with and predictive of psychological distress in terminally ill cancer patients.

The purpose of the present study was to determine the prevalence of adjustment disorders, major depression, and PTSD among terminally ill cancer patients; to identify factors that are associated with, and that predict them; and to determine how the psychological distress changes longitudinally.

	PATIENTS AND METHODS

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Patients
Consecutive patients were recruited on registration with the Palliative Care Unit (PCU) of the National Cancer Center Hospital East (Chiba, Japan) between October 1997 and November 1999. The unit has an outpatient service and a 25-bed in-patient service. In principle, patients register with the out-patient service and are mainly admitted to the in-patient service for symptom management, terminal care, and respite care for the family.³⁷ The eligibility criteria for patient recruitment in the study were: 1) age 18 years or older, 2) being newly registered with the PCU, 3) not currently undergoing curative cancer therapy, such as surgery, chemotherapy, or radiotherapy, 4) knowledge of the cancer diagnosis, 5) being not too ill to complete the questionnaires and participate in an interview taking at least 30 minutes, 6) not suffering from cognitive impairment, and 7) having no difficulty in verbal communication. While the "not too ill" criterion was judged by palliative care physicians, the physicians and investigators frequently provided feedback to each other and discussed eligibility on a case-by-case basis to avoid biased judgment and selection bias. Each patient was screened for cognitive impairment by means of the Japanese version of the Mini-Mental State Examination (MMSE; a score of 24 or more was the criterion for eligibility).^38,39

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 Helsinki Declaration. Written informed consent was obtained from each subject before the start of this study.

Assessment of Adjustment Disorders, Major Depression, and PTSD
The subjects were assessed for the presence of adjustment disorders and major depression by a trained psychiatrist using the Structured Clinical Interview for DSM-IIIR⁴⁰ at the time they registered with the PCU (baseline) and again when they were admitted to the PCU (follow-up). Subjects were evaluated for both cancer-related and non–cancer-related PTSD at baseline by means of the Structured Clinical Interview for DSM-IV.⁴¹ A Japanese version of the Structured Clinical Interview for DSM-IIIR is available, but a Japanese version of the Structured Clinical Interview for DSM-IV is not. We therefore used the Structured Clinical Interview for DSM-IIIR to assess adjustment disorders and major depression in the present study. On the other hand, since no Structured Clinical Interview to assess PTSD was available, the authors translated the original Structured Clinical Interview for DSM-IV for PTSD into Japanese and used it to assess PTSD in this study. The reliability (kappa coefficient) of the interview ratings was: 0.65 for adjustment disorders, 0.87 for major depression, and not calculated for PTSD, because no cases were diagnosed with PTSD.

Associated Factors and Predictive Factors for Adjustment Disorders, Major Depression, and PTSD
Sociodemographic and biomedical factors (cancer site, brain metastasis, Karnofsky Performance Status,⁴² time since the cancer diagnosis, use of steroids, and past history of chemotherapy and radiotherapy) were investigated (Table 1). The four frequent and distressing physical symptoms, pain, dyspnea, fatigue, and constipation, were assessed by asking the patient to describe the severity of each on a scale of 1 (absent) to 5 (extreme).^43,44 Patients were asked for permission to draw a blood specimen to determine the serum calcium concentration (measured by SRL Inc, Tokyo, Japan), and the values obtained were adjusted by Payne's method (adjusted calcium [mg/dL] = calcium [mg/dL] – albumin [g/dL] + 4.0).⁴⁵

Study Procedures
After obtaining the patients' consent, a trained psychiatrist administered the MMSE. Eligible patients participated in the interview and completed the questionnaires at the first outpatient visit after registration (baseline). When admitted to the PCU, their physical condition was discussed by palliative care physicians, nurses, and investigators, and the MMSE was administered by a trained psychiatrist again to patients considered capable of participating in the follow-up investigation. Patients with an MMSE score of 24 or more participated in the interview and completed the questionnaires for the follow-up investigation within 1 week of their admission.

Statistical Analysis
To identify cross-sectional factors associated with psychological distress at baseline, the subjects were divided into two groups according to whether they had been diagnosed with an adjustment disorder, major depression, or PTSD at baseline, and all of the variables investigated except the HADS score were included in the preliminary bivariate analysis, as appropriate. To identify the final associated factors, variables having a P value of less than .10 in the bivariate analysis were entered into a logistic regression model as independent variables. Similarly, to identify baseline predictive factors for psychological distress at follow-up, subjects who had completed the follow-up assessment were divided into two groups according to the diagnosis of adjustment disorder or major depression at follow-up, and the variables investigated were included in the preliminary bivariate analysis and logistic regression analysis. The analysis to identify predictive factors was performed on the cases with no psychiatric diagnosis at baseline. A P value of less than .05 was adopted as the significance level in all of the statistical analyses, and all P values reported are two-tailed. All statistical procedures were conducted with the SPSS version 10.0J software for Windows (SPSS Inc, Chicago, IL).

	RESULTS

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A total of 764 cancer patients registered with the PCU during the study entry period, but 507 of them were ineligible (too ill, n = 443; cognitive impairment, n = 50; and so on), and 278 (63%) of 443 patients judged to be "too ill", died within 2 weeks after registration with the PCU. Of the 257 eligible patients, 28 refused to participate and 20 could not be contacted (eg, because of emergency admission to another hospital), and 209 patients (27.4%) participated in the baseline assessment (Table 2). The patients' demographic data, such as age, sex, and cancer site, were similar to those of patients receiving palliative care in Japan,^50,51 and their social status, based on education, marital status, and household size, was also similar to most Japanese cancer patients.⁴⁹ Subsequent to the baseline investigation, 37 patients were not admitted to the PCU (eg, because of emergency admission to another hospital), and the other 172 were admitted to the PCU. However, six of them refused to cooperate further and 81 were judged to be ineligible (too ill, n = 57; cognitive impairment, n = 24). Thus, 85 of the subjects ultimately completed the follow-up assessment.

To assess longitudinal changes in performance status and physical symptoms among the 85 subjects who participated in the follow-up study, we investigated within-patient differences between the data from the baseline investigation and the follow-up investigation. The results of the analysis (Wilcoxon two-sample test) indicated that performance status (P < .001), pain (P = .03), and fatigue (P < .001) were significantly worse in the follow-up investigation than in the baseline investigation, while dyspnea (P = .24) and constipation (P = .1) did not change significantly.

The median interval and mean (standard deviation) interval between the baseline and follow-up assessment were 58 days and 103 (119) days, respectively, and the intervals ranged from 7 to 622 days. The median/mean survival time estimated by the Kaplan-Meier method after the baseline assessment and follow-up assessment were 100 and 229 days and 45 and 75 days, respectively.

Prevalence of Adjustment Disorders, Major Depression, and PTSD
At the baseline assessment, adjustment disorders were diagnosed in 34 patients (16.3%; depressed mood in 11.5%, anxious mood in 0.5%, mixed emotional features in 4.3%), major depression in 14 patients (6.7%), and PTSD in none (since none of first 100 consecutive patients was diagnosed with PTSD, we stopped assessing them for PTSD to lessen patients' burden.). At the follow-up investigation (n = 85), nine of the patients were diagnosed with adjustment disorders (10.6%; depressed mood in 4.7%, anxious mood in 3.5%, mixed emotional features in 2.4%), and 10 patients (11.8%) with major depression.

Factors Associated With Adjustment Disorders and/or Major Depression
Younger age, longer education, lower performance status, more severe pain, more severe constipation, more severe fatigue, greater concerns about financial issues, pain, being a burden to others, loss of independence and dignity, less satisfaction with confidantes, and presence of past history of major depression were significant factors associated with the presence of psychological distress (Table 1). The logistic regression analysis showed that lower performance status, greater concern about being a burden to others, and less satisfaction with confidantes were the final significant factors associated with the presence of psychological distress at baseline (Table 3).

Predictive Factors for Adjustment Disorders and/or Major Depression
The results of the bivariate analysis indicated only higher total HADS score as a baseline predictive factor for subsequent presence of adjustment disorders and/or major depression (Table 4), and it was also significant in the multivariate analysis after adjusting for the interval between the baseline and follow-up investigation (data not shown).

	DISCUSSION

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The results of the structured psychiatric interview indicated that approximately one-fourth of the terminally ill cancer patients experienced adjustment disorders and/or major depression. On the other hand, the results also suggest that few of them experienced PTSD, although no definitive conclusion about the prevalence of PTSD in terminally ill cancer patients can be drawn, because we stopped assessing PTSD at the first 100 patients and did not assess PTSD during the follow-up. The results of a recent systematic review of depression in terminally ill cancer patients suggested that at least 30% experience clinical depression, including major depression, and adjustment disorders.⁵² Our findings indicate that the prevalence rate of adjustment disorders and/or major depression may be somewhat lower than estimated; however, they need to be interpreted carefully in light of the limitations of selection bias. Nevertheless, in view of the prevalence rate of major depression in Asian general populations (prevalence, 0.12% to 1.6%),^53-55 our findings suggest a high prevalence of major depression and adjustment disorders in terminally ill cancer patients.

Since several studies that have used psychiatric interviews to assess PTSD in cancer patients have shown low prevalence rates of PTSD (ranging from 3% to 35%),^19,21-24 PTSD morbidity seems rare in cancer patient populations. Thus, our findings suggest that, in contrast to other potentially traumatic events, such as rape, physical assault, and combat, which frequently cause PTSD,⁵⁶ cancer-related experiences themselves may not be common traumatic events that result in a clinical diagnosis of PTSD.

The findings in our study regarding factors associated with adjustment disorders and/or major depression indicate that multidimensional factors, such as physical functioning, social support factors, and existential issues, may underlie the psychological distress experienced by terminally ill cancer patients. This suggests that comprehensive care, including physical, psychosocial, and existential dimensions, is indispensable for these patients. Because both conventional pharmacotherapy and psychotherapy are useful in ameliorating psychological distress in cancer patients,^57-59 and some recent papers have described new treatment modalities, such as "meaning-centered psychotherapy" and "dignity psychotherapy" in the care of terminally ill patients with existential distress,^60,61 appropriate combinations of these therapies seems promising. The absence of any association between the use of steroids and psychological distress may be an additional important finding, because steroids are widely used in palliative care settings.^62,63 Our findings suggest that use of steroids may not be associated with deterioration of patients' psychological status.

Despite the relatively short interval between the baseline and follow-up investigation (median, 58 days), the clinical course of the adjustment disorders and/or major depression seems to have been variable. In fact, more than 30% of the patients showed some change in psychological status, suggesting that continuous, close, and intensive monitoring of psychological distress is required in terminally ill cancer patients.

The results of this study showed that only the self-report anxiety and depression score can predict subsequent adjustment disorders and/or major depression in patients without clinical psychological distress at baseline, suggesting that even when anxiety and depression are on a subclinical level, they should be managed intensively to prevent subsequent psychological distress. Several studies have demonstrated that psychotherapeutic intervention, both individual and group, can be effective in reducing psychological distress among patients with terminal cancer and metastatic breast cancer,^58,59 and thus psychotherapy is a promising preventative strategy. Since a recent study has demonstrated that the widely used antidepressant fluoxetine, a selective serotonin-reuptake inhibitor, is not only useful in reducing depressive symptoms but well tolerated in advanced cancer patients screened for at least minimal depressive symptoms, pharmacotherapy also appears promising.⁶⁴

Finally, we would like to mention the potential influence of other cultural differences on the findings obtained. In general, Japanese society is characterized by a low divorce rate, stronger sense of belonging to a family than of being an individual, and low rate of active practice of religion. In fact, the patient's characteristics in the present study, including marital status, proportion of living alone, and religious practice, clearly differ from those of Western patients in similar settings.^9,13 These cultural features may have contributed to several of the findings obtained, including the somewhat lower prevalence of psychological distress and absence of any association between either loss of independence or loss of dignity and psychological distress.

Our study has several limitations. First, since only 27.4% (209 of 764 patients) of the subjects at baseline and 11.1% (85 of 764 patients) of the subjects at follow-up could be included in the analysis, generalizing the results may be impossible, and the sample size of the follow-up group was not very large. These limitations may have resulted in underestimation of the prevalence of the psychological distress and distortion of the associated and predictive factors. In addition, the fact that the patients who participated in the follow-up study were more likely to be female than those who did not participate indicates potential bias resulting from the observed sex differences. On the other hand, since a previous comprehensive review article and our baseline finding suggest that sex difference itself does not seem to impact the prevalence of psychological distress in cancer patients,⁶⁵ even though several papers in the literature suggest an effect of sex difference (see the Introduction section),³⁶ we do not think that this difference caused serious bias in our study. Additionally, the findings regarding within-patient differences between the baseline and the follow-up investigation suggest that the participants in the follow-up investigation experienced more stressful physical conditions than the participants in the baseline investigation. These findings suggest that the participants in the follow-up study were not an extremely biased sample. Second, the fact that the baseline investigation was cross-sectional in design precludes drawing any conclusions about causality. Third, since the study was conducted in one institution, institution bias may be another problem. Fourth, because the assessment of the physical symptoms and patients' concerns was conducted by an ad hoc method and the validity and reliability of the measures were not well established, they may have resulted in measurement errors. Fifth, potentially important information, including information on meaninglessness and hopelessness was lacking and may have distorted the results. Sixth, the timing of the follow-up assessment (admission) may also have produced distortions, because the reasons for admission may have differed. Finally, because this study focused on terminally ill cancer patients receiving palliative care, the results may not be applicable to patients with terminal cancer in other settings.

	Authors' Disclosures of Potential Conflicts of Interest

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The authors indicated no potential conflicts of interest.

	Acknowledgment

 
We thank Professor David W. Kissane, Centre for Palliative Care, University of Melbourne, for his helpful comments on the paper, and we also thank Yurie Sugihara and Ryoko Katayama for their research assistance.

	NOTES

 
Supported in part by a Grant-in-Aid for Cancer Research (11-2) from the Japanese Ministry of Health, Labor and Welfare, and a Grant-in-Aid for Scientific Research from the Japanese Ministry of Education, Culture, Sports, Science and Technology. Toru Okuyama and Yuriko Sugawara are awardees of a Research Resident Fellowship from the Foundation for Promotion of Cancer Research in Japan.

This work was carried out at the Psycho-Oncology Division, National Cancer Center Research Institute East, Chiba, Japan.

Authors' disclosures of potential conflicts of interest are found at the end of this article.

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Submitted August 22, 2003; accepted February 23, 2004.

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