Originally published as JCO Early Release 10.1200/JCO.2007.11.8844 on August 11 2008

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Better Off Dead: Suicidal Thoughts in Cancer Patients

Jane Walker, Rachel A. Waters, Gordon Murray, Helen Swanson, Carina J. Hibberd, Robert W. Rush, Dawn J. Storey, Vanessa A. Strong, Marie T. Fallon, Lucy R. Wall, Michael Sharpe

From the University of Edinburgh Cancer Research Centre, School of Molecular and Clinical Medicine, University of Edinburgh; the Edinburgh National Health Service Cancer Centre, Edinburgh, Scotland; and the Centre for Statistics in Medicine, University of Oxford, Oxford, United Kingdom

Corresponding author: Jane Walker, 8th floor, Kennedy Tower, Royal Edinburgh Hospital, Edinburgh, United Kingdom EH10 5HF; e-mail: jane.walker{at}ed.ac.uk

	ABSTRACT

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Purpose: Cancer is associated with an increased risk of suicide and attempted suicide. However, we do not know how many cancer patients have thoughts that they would be better off dead or thoughts of hurting themselves. This study aimed to determine the prevalence of such thoughts in cancer outpatients and which patients are most likely to have them.

Patients and Methods: A survey of consecutive patients who attended the outpatient clinics of a regional cancer center in Edinburgh, United Kingdom. Patients completed the Patient Health Questionnaire-9 (PHQ-9), which included Item 9 that asks patients if they have had thoughts of being better off dead or of hurting themselves in some way in the previous 2 weeks. Those who reported having had such thoughts for at least several days in this period were labeled as positive responders. Patients also completed the Hospital Anxiety and Depression Scale (HADS) and a pain scale. The participating patients’ cancer diagnoses and treatments were obtained from the cancer center clinical database.

Results: Data were available on 2,924 patients; 7.8% (229 of 2,924; 95% CI, 6.9% to 8.9%) were positive responders. Clinically significant emotional distress, substantial pain, and—to a lesser extent—older age, were associated with a positive response. There was strong evidence of interactions between these effects, and emotional distress played the most important role.

Conclusion: A substantial number of cancer outpatients report thoughts that they would be better off dead or thoughts of hurting themselves. Management of emotional distress and pain should be a central aspect of cancer care.

	INTRODUCTION

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Advances in cancer treatments have improved the prognosis and quality of life of many patients, but cancer is still associated with an increased rate of suicide^1-14 and of attempted suicide.¹⁵ One method of suicide prevention is to identify those patients who have thoughts that may lead to a suicide attempt, such as of being better off dead or of hurting themselves. Patients with medical conditions are more likely than the general population to report having these types of thoughts.¹⁶ In cancer patients, however, published studies have only been of subgroups, such as those with terminal cancer^17-21 or those referred to psychiatric services.^22-25 Therefore, we do not know what proportion of general cancer outpatients have such thoughts and which of these patients are most likely to have them.

The nine-item Patient Health Questionnaire (PHQ-9) is a validated and widely used self-report screening tool for major depressive disorder in patients who attend medical services.²⁶ We used responses to Item 9 on this scale, which asks about thoughts of being better off dead and thoughts of hurting yourself in some way, to determine the prevalence of such thoughts in cancer outpatients. We also examined the association of demographic and clinical variables with these thoughts.

This report is one of a series of reports that is based on the analysis of routinely collected data on consecutive outpatients who attend the Edinburgh Cancer Centre.²⁷

	PATIENTS AND METHODS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS Appendix REFERENCES

 
Design
A cross-sectional survey.

Patients
The study took place in the outpatient department of the Edinburgh Cancer Centre, a regional cancer center that is the sole provider for specialist cancer services to a geographically defined area of approximately 1.5 million people in the southeast area of Scotland, United Kingdom. We surveyed a consecutive series of patients who attended the outpatient department between June 2003 and December 2004 in the following cancer clinics: colorectal, gynecologic, genitourinary, sarcoma, melanoma, breast, and miscellaneous. Patients were excluded from screening if they were attending the clinic for their initial assessment, were too ill, had cognitive impairment, or had severe communication difficulties.

Measures
Patient health questionnaire-9. The Patient Health Questionnaire-9 (PHQ-9) is a self-report scale comprised of nine items that relate directly to each of the nine symptoms of major depressive disorder as defined by the Diagnostic and Statistical Manual of Mental Disorders, fourth edition (DSM-IV).²⁸ Each of the nine items is scored from zero to three, which results in a maximum summed score of 27; higher scores represent an increased severity of depression. Item 9 asks, "Over the last two weeks how often have you been bothered by the following problem: thoughts that you would be better off dead, or of hurting yourself in some way?" Patients may respond with the following answers: "not at all" (scoring zero), "several days" (scoring one), "more than half the days" (scoring two) or "nearly every day" (scoring three). Patients who reported such thoughts for at least several days in this period (ie, those who scored one or more on Item 9) were labeled positive responders.

Cancer Center Clinical Database. The clinical database contained patients’ demographic and clinical details, including cancer diagnoses, clinical staging of disease, and treatment received.

Hospital Anxiety and Depression Scale. The Hospital Anxiety and Depression Scale (HADS)²⁹ is a 14-item self-report scale, and it has two subscales (which measure anxiety and depression) that each contain seven items. In practice, the two subscales correlate highly and are commonly used as a single measurement of emotional distress. Individual items are each rated on a four-point scale that is scored from zero to three, which results in maximum subscale scores of 21 and a total score of 42. Patients were asked to rate their symptoms during the preceding week. Before analysis, we defined clinically significant emotional distress as a HADS total score of 15 or more. This cutoff has been reported to offer good sensitivity and specificity for anxiety and depressive disorders in patients with cancer.^30,31

European Organisation for Research and Treatment of Cancer Quality of Life Questionnaire-C30 Severity of Pain Item. The European Organisation for Research and Treatment of Cancer Quality of Life Questionnaire-C30 (EORTC QLQ-C30)³² is a self-report questionnaire that is designed to measure health-related quality of life in cancer patients. The questionnaire asks patients about their health during the preceding week and includes a two-item scale that measures pain. We used the EORTC Scoring Manual to transform pain scores to a scale of 0 to 100 and, before analysis, defined substantial pain as a score of 50 or greater.³³

Procedure
Semi-automated symptom screening has been established in the Edinburgh Cancer Centre as part of routine clinical practice. Consecutive outpatients were invited to complete the PHQ-9, the HADS, and the EORTC QLQ-C30 pain items. Patients completed the questionnaires by using touch-screen computers before their oncology consultation. An assistant was present to guide patients who needed help using the computers, and the results of each screening episode were provided to the patient's oncologist before the consultation. The data were also stored on a database and form the basis of this report.

Ethical Approval
As the data were collected as part of the clinical service, consent was not obtained from individual patients. Approval for the aggregated anonymized data to be reported was obtained from the local research ethics committee.

Data and Analysis
Patients took part in symptom screening on each reattendance at the cancer center. As the frequency of visits varied between patients and clinics, only the data collected from each patient's first screening within the study period was used in the analysis.

The clinical data relevant to each patient at the time of screening were obtained from the cancer center clinical database. These data were anonymized and were matched to the patient's questionnaire response by merging the two databases using a unique patient identification number and date of birth. Patients who were not listed on the database were excluded from the analyzed sample. Patients who were not married or did not have a partner were classified as unmarried. Cancer type was classified according to the site of origin; when there was more than one cancer type, the cancer dominating treatment at the time was recorded. Disease status was classified as either disease free or active disease. Treatment status was defined as treatment the patient had received in the 2 months before screening and was categorized as no anticancer treatment, receiving hormone treatment, or receiving chemotherapy and/or radiotherapy treatment (Appendix). The accuracy of data obtained from the clinical database was checked against a 5% random sample of paper case notes, and good agreement (93%) of classification categories was found.

The statistical analysis first compared the characteristics of eligible patients who had complete data with those patients who refused screening or had missing PHQ-9 Item 9 data to determine to what extent the analyzed sample was representative. The prevalence of positive responders was then calculated. The associations of a positive response with the following variables were analyzed—first by using univariate logistic regression, then by using multivariate logistic regression with the method of stepwise selection: age, sex, marital status, primary cancer diagnosis, disease status, treatment status, clinically significant emotional distress, and substantial pain.

	RESULTS

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Characteristics of the Sample
Data were available on 2,924 patients, which represented 84% of patients potentially eligible for inclusion in the analysis. The details of how the final sample was derived and the reasons for missing data are shown in Figure 1.

View larger version (31K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 1. Flow diagram to illustrate the derivation of the sample. (*) Patients unable to complete screening had communication difficulties, cognitive impairment, or were too ill. () Patients refused to participate in screening or were not approached due to busy clinics. PHQ-9, Patient Health Questionnaire-9.

Association of Demographic and Clinical Characteristics With a Positive Response to Item 9
Univariate logistic regression was used to investigate associations between positive responses and patients’ demographic and clinical characteristics. The results of this analysis are reported in Table 2. Patients were more likely to be positive responders if they were unmarried, had active disease, had clinically significant emotional distress, or had substantial pain; the latter two variables had larger effects.

	DISCUSSION

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Study Limitations
This is, to our knowledge, the first study to report the prevalence of thoughts of being better off dead or thoughts of hurting yourself in cancer outpatients. The study has three main limitations: The first limitation concerns the generalizability of the findings. We surveyed patients in a specialist cancer center in the United Kingdom, the symptom screening service was not available in all clinics, and some patients either refused or were too unwell to participate. The findings of this study, therefore, may not be typical of other cancer services. The second limitation concerns the measure. As we used a self-completed screening measure, rather than an interview, we had to rely on the patient's interpretation of the question. The question selected (Item 9 of the PHQ-9) did not ask patients specifically about thoughts of attempting suicide. However, the use of a more specific item, such as the suicidal intent item of the Beck Depression Inventory³⁴ was considered likely to lead to increased refusal of patients to participate in screening. The third limitation concerns the data available for analysis, which were obtained from patients who participated in routine symptom screening. These were cross-sectional and did not include all the factors that may be associated with thoughts of being better off dead or of hurting yourself, such as the patients’ general health and their social supports.³⁵

Comparison With Other Studies
There have been a number of other studies of the prevalence of individuals who report thoughts of being better off dead and of suicidal ideation. The latter term can be defined in a number of ways that range from intermittent suicidal thoughts without any intent to act to constant thoughts and plans to commit suicide. Studies of suicidal ideation have reported a range of prevalence estimates, which reflects the different screening tools used, the varying time periods patients were asked to report on (eg, last 2 weeks to lifetime), and the range of populations in which the studies were carried out.

In the general population, the prevalence of individuals who experience suicidal ideation has been reported as 2% to 25%.^36-41 A study of a large South Australian community sample that used Item 9 of the PHQ-9 reported a 2.6% prevalence of positive response, which, as expected, is lower than that found in our sample of cancer outpatients.⁴² This suggests that cancer patients have three times the general population risk of suicidal ideation.

Patients who have medical illnesses have been reported to have a higher rate of suicidal ideation than the general population.¹⁶ A study of patients who attended a neurology clinic and completed Item 9 of the PHQ-9, followed by a clinical interview, reported that 9% of patients experienced significant suicidal ideation⁴³—a figure similar to the 8% we found in this study.

We are not aware of any studies that are directly comparable to this one. However, a high desire for death or thoughts of suicide has been reported in up to 31% of terminally ill cancer patients,^17-21,44 and suicidal ideation has been reported in more than one half of cancer patients referred to a psychiatric service with a diagnosis of depression.^23,24

Clinically significant emotional distress, substantial pain, and—to a lesser extent—older age were the only variables associated with suicidal ideation in this study, and emotional distress far outweighed the others in its strength of association. Distress and depression have been reported previously as risk factors for suicidal thoughts in cancer patients.^17,21-24 Pain has been associated with high desire for death in the terminally ill,²⁰ and it is the most common reason for suicidal thoughts given by those cancer patients who considered suicide a possible future option.¹⁸ These risk factors of emotional distress and pain are themselves interrelated.⁴⁵ Finally, older age has also been associated with suicidal ideation in depressed cancer patients.²⁴

In summary, previous studies in small, selected samples have suggested that suicidal ideation is more common in cancer patients than in the general population and that emotional distress, pain, and age are risk factors. The current study of a large representative sample of cancer outpatients provides more robust support for these observations.

Implications for Practice
Although progress has been made in prolonging and improving the quality of life of patients with cancer, this survey reveals that a substantial number of patients report thoughts of being better off dead or thoughts of hurting themselves. This is a sobering finding, and it clearly requires further investigation.

Although the majority of patients who report suicidal thoughts will not attempt suicide,⁴⁶ further assessment is necessary to identify those who are at high risk of doing so. This assessment may, in the first instance, be carried out by appropriately trained oncology clinicians who are guided by a protocol and who have supervision and advice available from a psychiatrist.

Suicidal thoughts are most common in those cancer patients who have emotional distress and substantial pain. This finding suggests that the identification of and treatment of these symptoms may not only improve a cancer patient's quality of life but also contribute to reducing the risk of suicide.

	AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS Appendix REFERENCES

 
The authors indicated no potential conflicts of interest.

	AUTHOR CONTRIBUTIONS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS Appendix REFERENCES

 
Conception and design: Jane Walker, Michael Sharpe

Collection and assembly of data: Helen Swanson, Carina J. Hibberd, Dawn J. Storey, Vanessa A. Strong, Lucy R. Wall

Data analysis and interpretation: Jane Walker, Rachel A. Waters, Gordon Murray, Carina J. Hibberd, Robert W. Rush, Michael Sharpe

Manuscript writing: Jane Walker, Dawn J. Storey, Michael Sharpe

Final approval of manuscript: Jane Walker, Rachel A. Waters, Gordon Murray, Helen Swanson, Carina J. Hibberd, Robert W. Rush, Dawn J. Storey, Vanessa A. Strong, Marie T. Fallon, Lucy R. Wall, Michael Sharpe

	Appendix

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION AUTHORS' DISCLOSURES OF... AUTHOR CONTRIBUTIONS Appendix REFERENCES

 
Cancer and Treatment Status Classifications
Primary cancer at the time of screening. Because of the small numbers of patients in some categories, the primary cancer diagnoses were grouped into seven major categories: breast, bowel (which included rectal, colon, and anal sites of origin), other gynecologic (which included cervical, uterine, vulva, and vaginal sites of origin), testicular, prostate, and miscellaneous (which included lymphoma, head and neck, lung, upper gastrointestinal, melanoma, brain and central nervous system, kidney, adrenal gland, bladder, epididymis, sarcoma, primary peritoneal, basal cell, and unknown primary cancers).

In the majority of the patients, the primary cancer diagnosis was classified according to the site of origin. The only exceptions were as follows: (1) melanoma, classified as melanoma regardless of the site of origin; and (2) germ cell tumor in regions other than the gonads (eg, mediastinal), classified in men as testicular and in women as ovarian cancer.

Those patients who had had more than one primary cancer diagnosis were classified according to the cancer they were being treated for at the time of screening. If they were being treated for more than one malignancy concurrently, they were classified according to the cancer diagnosis that was dominating their treatment at the time of screening. Those patients who were disease free and were on no treatment for any of their previous cancers were classified according to their most recently diagnosed cancer.

Disease Extent at Time of Screening
Patients were classified according to the extent of clinically detectable disease at the time of screening. The categories were disease free, active disease, or unknown. Some clinical situations could be classified in more than one way. For clarity, these are outlined in the appropriate section.

Disease-Free Classification
(1) Postsurgical adjuvant radiotherapy/chemotherapy/hormone therapy with no clinically detectable residual disease; (2) postcompletion of primary radical chemotherapy or radiotherapy given with curative intent, and no documented residual disease or recurrence (ie, early anal cancer after radical chemoradiotherapy and stage III ovarian cancer after chemotherapy with normal serum tumor markers); and (3) metastatic cancer that had been surgically removed, and no documentation of recurrence (eg, liver metastases from bowel cancer that were removed after chemotherapy and partial hepatectomy).

Active Disease (Local and Metastatic Disease Categories Combined) Classification
Local disease. (1) Clinically detectable local disease or regional lymph node metastases; (2) primary chemotherapy or radiotherapy with curative intent (eg, early anal cancer); and (3) neoadjuvant chemotherapy/radiotherapy/hormone treatment before surgery (unless metastatic disease).

Metastatic disease. (1) Metastases to organs or to distant lymph nodes; (2) stage III ovarian cancer that was treated with primary or postsurgical chemotherapy at the time of screening (because of the assumption of residual disease in the abdominal cavity); (3) relapsed ovarian cancer; (4) primary lung cancer with disease in more than one lobe of lung (because not treated with curative intent); and (5) breast cancer with supraclavicular nodes.

Unknown Classification
Unknown classification assigned when it was unclear what the cancer status was at the time of screening.

Treatment Status at the Time of Screening
Treatment status was described according to what treatment had been received within the 2 months before screening: no prescribed anticancer treatment; hormone treatment; or chemotherapy, radiotherapy, surgery, or any combination of these (though this does not automatically imply that they were concurrent). These were collapsed into the three groups presented in the paper: (1) no prescribed anticancer treatment (which included those who underwent surgery), (2) hormone treatment, and (3) chemotherapy and/or radiotherapy treatment. Those who had received two treatment modalities within the last 2 months were allotted to the most clinically dominant category, according to the following ranking: chemotherapy/radiotherapy greater than hormone therapy greater than surgery. For example, those who had received both surgery and chemotherapy were assigned to the radiotherapy and/or chemotherapy treatment group.

No distinction was made between the dose and the fractionation of radiotherapy administered; patients were classed as undergoing radiotherapy if at least one fraction of treatment had been administered within the previous 2 months.

The arbitrary 2-month cutoff was made on the basis that patients’ symptoms might still be affected by treatment, such as chemotherapy, that was completed several weeks before screening. The authors recognize that possible treatment-associated symptoms may resolve before or after this time.

	ACKNOWLEDGMENTS

 
We thank Elspeth Currie, Sarah Hoskin, Sarah Humble, Ian MacDonald, Joerg Sigle, and Jackie Whigham for valuable assistance in conducting this research and Nav Kapur, Keith Hawton and Kurt Kroenke for helpful advice on the interpretation of the findings.

	NOTES

 
published online ahead of print at www.jco.org on August 11, 2008

Supported by Cancer Research United Kingdom.

Authors’ disclosures of potential conflicts of interest and author contributions are found at the end of this article.

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Submitted March 24, 2007; accepted October 11, 2007.

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