Support Care Cancer (2012) 20:2795–2802 DOI 10.1007/s00520-012-1401-3

ORIGINAL ARTICLE

Frequency of depression among oncology outpatients and association with other symptoms Wadih Rhondali & Elise Perceau & Julien Berthiller & Pierre Saltel & Veronique Trillet-Lenoir & Olivier Tredan & Jean-Pierre Coulon & Eduardo Bruera & Marilene Filbet

Received: 2 August 2011 / Accepted: 3 February 2012 / Published online: 17 February 2012 # Springer-Verlag 2012

Abstract Purpose Depression occurs among an estimated 15% of cancer patients (range, 1–77.5%). Our main objective was to identify the frequency of reported depression by using the Brief Edinburgh Depression Scale (BEDS) among cancer outpatients. Our secondary objective was to identify associated symptoms of cancer using the Edmonton Symptom Assessment System (ESAS) and to evaluate the screening performance of depression between ESAS and BEDS. Methods In this multicenter prospective study conducted, we used the ESAS to collect information on nine symptoms: pain, fatigue, nausea, depression, anxiety, drowsiness, shortness of breath, lack of appetite, and feeling of well-being (each rated from 0 to 10). The BEDS was used to assess for

W. Rhondali (*) : E. Bruera Department of Palliative Care and Rehabilitation Medicine, Unit 1414, The University of Texas MD Anderson Cancer Center, 1515 Holcombe Boulevard, Houston, TX 77030, USA e-mail: [email protected] W. Rhondali : E. Perceau : V. Trillet-Lenoir : M. Filbet Centre Hospitalier de Lyon-Sud, Hospices Civils de Lyon, Lyon, France J. Berthiller Pole Information Médicale Evaluation Recherche, Hospices Civils de Lyon, Lyon, France P. Saltel : O. Tredan Centre Léon Bérard, Lyon, France J.-P. Coulon Clinique Francois Chenieux, Limoges, France

“probable depression” (score >6). Data were analyzed using a parametric and nonparametric test. Results A total of 146 patients completed the study. The prevalence of probable depression was 43/146 (29%). Probable depression was associated with increased fatigue (p0 0.008), depression (p<0.0001), anxiety (p<0.0001), shortness of breath (p00.01), and decreased feeling of well-being (p<0.001). Among patients with probable depression, 42 (98%) patients were not using antidepressants. Regarding the sensitivity and the specificity, we determined that the optimal cutoff for using the ESAS as a depression screening tool was ≥2. Conclusion We found significant associations between probable depression as determined with the BEDS and five symptoms as detected with the ESAS. The vast majority of patients with probable depression were not receiving pharmacological treatment. Depression should be suspected in patients with higher symptom distress as for any one of these 5 ESAS items. Keywords Depression . Cancer . Outpatient . Screening

Introduction Progress in cancer treatment has led to a substantial numbers of patients who are reaching increased longevity. For this reason, more attention has been given to psychological symptoms [1]. Depression is a frequent problem among cancer patients and has been estimated to occur with a frequency of approximately 15% (range, 1–77.5%) [2–5]. Depression is often under-diagnosed and hence, undertreated [6–8], even though the benefit of such treatment has been well established for both depression symptoms

2796

Support Care Cancer (2012) 20:2795–2802

[9–12] and physical symptoms such as pain, sleep disturbances, and anorexia [13]. One explanation for this under-recognition of depression is that cancer patients experience neurovegetative symptoms that simulate several symptoms caused by cancer or the treatment (e.g., loss of appetite, fatigue, and sleep disturbances). Furthermore, compared with pain assessments, emotional well-being is significantly less likely to be documented in medical records, suggesting that psychological distress is less likely to be assessed than physical distress is [14]. However, depression leads to a reduction in quality of life as well as the aggravation of physical symptoms such as pain, fatigue, and sleep disturbances [15, 16]. In addition, advanced cancer patients reporting higher physical distress on the Edmonton Symptom Assessment System (ESAS) (e.g., nausea, fatigue, drowsiness, and worse appetite) are more likely to report a higher level of depression [17, 18]. Depression has also been reported to reduce adherence with cancer treatment and prolong hospitalization [9, 19–22]. Moreover, depression is an independent predictive risk factor for cancer-related mortality [23, 24]. The National Comprehensive Cancer Network guidelines for distress management recommend that all cancer patients be screened for their level of distress at the initial visit with their oncologist by using screening tools [22]. Despite the growing acknowledgment of the importance of depression among cancer patients and the recommendations of national and international organizations for systematic screening and active management of depression, implementation of these screening tools in daily clinical practice remains minimal [14, 25]. A recent study that explored the barriers that oncologists and palliative care clinicians might experience in diagnosing depression found that lack of time was the main barrier [26]. In addition, the providers had difficulty applying diagnostic criteria for depression for the general population to cancer patients, mainly for the nonspecific symptoms as fatigue, anorexia, and feelings of guilt. This reported lack of time and difficulty in applying general diagnostic criteria to a more specific population has generated a growing interest in the development and the implementation of screening and assessment tools to improve the accuracy of detecting depression among persons with cancer [1, 8, 22, 27–29].

Screening tools are more likely to be used if they are easy to administer and score without specialized training and if patients find them acceptable (e.g., time to complete, ease of use if self-administered, discomfort, and embarrassment). [30]. Furthermore, the tools should be as concise as possible and exclude physical indicators insofar as possible. Currently, few screening questionnaire (Brief Edinburgh Depression Scale (BEDS), Edmonton Symptom Assessment System (ESAS), Hospital Anxiety and Depression Scale, Beck Depression Inventory, Edinburgh Depression Scale, Distress Thermometer) meets these ideals for identifying depression among cancer patients (Table 1). The BEDS was developed from the Edinburgh depression scale (EDS). The BEDS is an abbreviated 6-item version that has been developed and validated for patients with advanced cancer [31]. With that patient population, the BEDS demonstrated good internal consistency, and the study results suggested that a small number of items are preferable for screening patients who are weak and unwell [31]. The 6-item BEDS is a commonly used screening tool because of its efficacy in detecting depression—the most valid cutoff score (out of 18) is 6 for a sensitivity of 72% and specificity of 83%—and its acceptability to patients [31]. This English-language scale had initially been designed for use with cancer outpatients. We recently translated the scale into French and validated its use with inpatients with advanced cancer [32]. Our main objective was to identify the frequency of reported depression by using the BEDS among cancer outpatients. Our secondary objective was to identify associated symptoms of cancer using the ESAS and to evaluate the screening performance of depression between ESAS and BEDS.

Materials and methods This study was approved by the local ethics committee and the Institutional Review Board of the coordinating center (Hospices Civils de Lyon) in compliance with French law and the Declaration of Helsinki. Computerized data were processed anonymously. Written information about the

Table 1 Comparison of different screening tools for depression

Easy to use Efficacy Acceptability Cost

Single item

Depression ESAS item (≥20 mm)

No instruction ++++ Se00.55 Sp00.74 ++++ Low

Initial instruction +++ Se00.77 Se00.76 Sp00.55 Sp00.82 ++++ ++++ Low Low

Se sensitivity, Sp specificity

Distress thermometer (≥4)

BEDS (6 items) (≥6)

EDS (10 items) (≥13)

Initial instruction ++ Se00.72 Se00.70 Sp00.83 Sp00.80 +++ ++ Low Low

HADS (14 items) (≥20)

BDI (21 items) (≥8)

Se00.77 Sp00.89 ++ Low

Se00.79 Sp00.71 + Low

Support Care Cancer (2012) 20:2795–2802

study and its aim was given to all participants, and all gave written consent before they were enrolled in the study. This prospective multicenter study was conducted at three institutions in France that treated cancer patients on an outpatient basis from May through July 2009. We chose to conduct this study in three different settings in order to collect data representing a wider spectrum of cancer patients. The settings were the comprehensive cancer center Centre Leon Berard, the medical oncology unit at the university hospital Centre Hospitalier Lyon-Sud, Hospices Civils de Lyon, and the private cancer clinic Clinique Francois Chenieux in Limoges. Participants We included in our assessment all the consecutive outpatients during 1 week at the university hospital and at the private clinic (the last week of May and July 2009, respectively). The comprehensive cancer center treated a greater number of patients (almost 100 patients per day). We selected 20 patients per day using a random number generator because each day was scheduled for the treatment of a specific type of tumor, and we were looking to be as representative as possible of the outpatient population. Furthermore, we did not have the logistical resource to screen a large number of patients in 1 day. The only exclusion criteria was a performance status score ≥3 assessed using the Zubrod score [33]. We chose to include only patients with a low level of functional impairment to keep our sample homogenous. Procedure Patients were recruited and interviewed before their consultation with their oncologist. For each patient, we documented from the medical chart age, sex, primary cancer diagnosis, extent of cancer disease (metastasis), and time from the cancer diagnosis. We directly asked each patient about education level, marital status, personal and family history of depression, and current use of psychotropic medication (i.e., antidepressants or anxiolytics). Measures The ESAS is one of the most commonly used tools for clinical care in cancer [34]. The validated self-assessment tool ESAS was used to measure the intensity of nine symptoms experienced in the previous 24 h (pain, fatigue, nausea, depression, anxiety, drowsiness, shortness of breath, lack of appetite, and feeling of well-being) [35, 36]. This 11-point numeric rating scale, ranging from 0 (no symptom) to 10 (worst possible symptom), yields a total score and two subscale scores. These scores have been validated for

2797

patients with advanced cancer [37, 38]. The total symptom distress score is the sum of the scores for all nine symptoms; the possible total score can range from 0 to 90 [35]. The physical distress subscore is the sum of scores for six symptoms (pain, nausea, tiredness, drowsiness, lack of appetite, and shortness of breath), and the psychological distress subscore is the sum of scores for the remaining three symptoms (depression, anxiety, and feeling of well-being) [39]. The ESAS is designed to document symptom profiles over time by repeated quantitative measurements of symptom intensity. It has been shown to have good reliability and validity when compared to other tools and good test–retest reliability [36, 40, 41]. We used the BEDS to screen patients for depression. The BEDS has been developed and validated for patients with advanced cancer [31]. With that patient population, the BEDS demonstrated good internal consistency and validity. The cutoff of six was associated with a sensitivity of 82.4%, specificity of 68.4% [32]. On the basis of a previous research, we defined a score of >6 (out of 18) as “probable depression” [31, 32]. Statistical analysis Categorical variables were expressed as number (n) and percentage. The hypothesis of normal distribution of quantitative variables was tested using the Kolmogorov–Smirnov test. Quantitative variables were expressed as mean ± standard deviation when the distribution was normal or median with first and third quartile when the distribution was not normal. Categorical variables were compared using the Fisher's exact test when the conditions of application of Chi-square test were not met. Quantitative variables were compared between groups using Student'st test after verification of equality of variances when data were normally distributed, and with the nonparametric test for independent series of Mann–Whitney (two-sided) when the hypothesis of normality of distribution was not verified. The quantification of the association between ESAS parameters and BEDS as binary variable (>6 cutoff) was determined using a logistic regression. First, the univariate analysis was conducted, and second, the multivariate analysis was completed using each significant variable of the univariate analysis with age and sex in the model. Finally, the prognostic value of the depression item of the ESAS questionnaire to detect the subject with a BEDS score greater than 6 (defined as the gold standard) was determine using sensitivity, specificity, positive and negative predictive value, and the area under the ROC curve. The test of the difference was considered statistically significant for risk of type set at 5% (p≤0.05). Statistical analyses were conducted using SAS version 9.1.3 (SAS Institute Inc, NC).

2798

Support Care Cancer (2012) 20:2795–2802

Results A total of 150 patients were eligible and were approached for the study, and 146 were enrolled (4 patients refused to participate because they were reluctant to be asked about

their mood). Two patients from the group with a BEDS score ≤6 did not complete the ESAS. Patient demographics are summarized in Table 2. The patients' median age was 59.5 years (range, 28–85 years). Ninety-three (63.7%) participants were female, 106 (73.6%)

Table 2 Demographic and clinical characteristics of cancer patients attending outpatient clinics, by BEDS score Variable

All patients (n0146) n (%)

BEDS score ≤6 (n0103) n (%)

BEDS score >6 (n043) n (%)

p value

Age (years) median (Q1–Q3) Female Married Missing Education High school or below College education Advanced education Missing Extent of cancer disease Unknown No metastasis Metastasis Primary cancer diagnosis Breast Genitourinary Gastrointestinal Respiratory Hematologic Bone Other

59.5 (51.8–70.6) 93 (63.7) 106 (73.6) 2

60.7 (53.3–71.3) 62 (60.2) 74 (72.5) 1

56.8 (47.0–70.0) 31 (72.1) 32 (76.2) 1

0.09a 0.17b 0.65b

44 (30.6) 79 (54.9) 21 (14.6) 2

30 (29.4) 57 (55.9) 15 (14.7) 1

14 (33.3) 22 (52.4) 6 (14.3) 1

0.89b

41 (28.1) 71 (48.6) 34 (23.3)

31 (30.1) 44 (42.7) 28 (27.2)

10 (23.3) 27 (62.8) 6 (13.9)

0.07b

53 (36.3) 39 (26.7) 36 (24.7) 5 (3.4) 4 (2.7) 2 (1.4) 8 (5.5)

35 (34.0) 26 (25.2) 31 (30.1) 4 (3.9) 3 (2.9) 0 (0.0) 4 (3.9)

18 (41.9) 13 (30.2) 5 (11.6) 1 (2.3) 1 (2.3) 2 (4.7) 4 (9.3)

0.37b 0.53b 0.02b 0.99c 0.99c 0.09c 0.23c

1 (0.7) 41 (27.6) 3 (2.1) 35 (24.1) 66 (45.5)

0 (0.0) 29 (28.2) 1 (1.0) 20 (19.4) 53 (51.5)

1 (2.4) 11 (26.2) 2 (4.8) 15 (35.7) 13 (30.9)

0.02c

1

0

1

67(46.2) 68 (46.9) 10 (6.9) 1

47 (46.1) 49 (48.0) 6 (5.9) 1

20 (46.5) 19 (44.2) 4 (9.3) 0

0.73b

32 (21.9) 45 (31.3) 2

18 (17.5) 26 (25.5) 1

14 (32.6) 19 (45.2) 1

0.04b 0.02b

14 (9.6)

13 (9.9)

1 (7.1)

0.99c

20 (71.4)

15 (68.2)

5 (83.3)

0.64c

Time from cancer diagnosis ≤3 months 3–6 months 7 months–1 year 1–2 years >2 year Missing Performance status score 0 1 2 Missing Depression history Personal history Family history Missing Drug treatments Antidepressants Anxiolytics a

Wilcoxon test

b

Chi-square test

c

Fischer's exact test; Q1–Q3; first and third quartiles

Support Care Cancer (2012) 20:2795–2802

2799

were married, and 79 (54.9%) were college-educated. Seventy-one (48.6%) patients had no metastasis, 53 (36.3%) were diagnosed with breast cancer, 39 (26.7%) with genitourinary cancer and 36 (24.7%) with gastrointestinal cancer. Sixty-six (45.5%) patients had been diagnosed at least 2 years previously, and 136 (92.4%) had a performance status score of 0 or 1. A personal history of depression was reported by 32 (21.9%) patients and a family history of depression by 45 (31.3%) patients. Furthermore, in Table 2, we also reported the association between BEDS score and patient characteristics. A familial and personal history of depression was associated with a higher risk (p00.02 and p00.04, respectively). In addition, a primary cancer diagnosis of gastrointestinal malignancy was associated with a lower risk of depression (p00.02). The BEDS score was not significantly associated with current use of antidepressants or anxiolytics. Table 3 reports the association between ESAS items and BEDS score. We found a significant correlation between the BEDS and the ESAS scores for increased fatigue (p00.008), increased depression (p<0.0001), increased anxiety (p< 0.0001), increased shortness of breath (p 00.01), and Table 3 Association between ESAS items and BEDS score

Variables

decreased feeling of well-being (p<0.0001). The BEDS score was also significantly correlated with the physical distress subscore (p00.009), the psychological distress subscore (p<0.0001), and the total symptom distress score (p< 0.0001) (Table 3). The multivariate analysis shows that anxiety was the most important risk factor after adjusting for age and sex (Table 4). We validated the ESAS depression item scores of ≥1, ≥2, ≥3, or ≥4 (out of a possible 10) against the BEDS score >6. Regarding the sensitivity and the specificity, we determined that the optimal cutoff for using the depression ESAS item as a depression screening tool was ≥2 (Table 5). For a score ≥2, ESAS was found to have a sensitivity of 0.73, a specificity of 0.74, a positive predictive value of 0.62, and a negative predictive value of 0.83.

Discussion According to the BEDS, 29% of this patient population had probable depression. However, the depressed patients were considerably under-treated with only one patient with a

All patients (n0146) n (%)

ESAS items [mean ± SD; median (Q1–Q3)] Pain 2.0 (0.4–4.5)

ESAS Edmonton Symptom Assessment System, PHS physical distress subscore, PSS psychological distress subscore, TSDS total symptom distress score, SD standard deviation, Q1–Q first and third quartiles a

Wilcoxon test

b

Student'st test

BEDS score ≤6 (n0103) n (%)

BEDS score >6 (n043) n (%)

p value

1.7 (0.4–4.0)

3 (0.5–5.6)

0.12a

Missing Fatigue Missing Nausea Missing Depression Missing Anxiety Missing Drowsiness Missing Shortness of breath Missing Lack of appetite Missing Well-being Missing PHS Missing

5 4.5 (2.0.0–6.8) 7 1.0 (0.0–2.8) 6 1.4 (0.2–3.2) 6 2.3 (0.5–4.5) 6 2.6 (0.5–5.4) 6 2.3 (0.5–4.5) 5 1.4 (0.0–4.5) 5 3.0 (0.8–4.9) 7 17.5±11.6 7

2 3.8 (1.5–6.7) 4 1.0 (0.0–2.7) 3 0.7 (0.0–2.3) 3 1.5 (0.0–2.9) 3 2.3 (0.4–5.4) 3 1.7 (0.4–3.7) 2 1.2−(0.0–4.0) 2 2.2 (0.5–4.5) 4 15.9±11.0 4

3 6.1 (3.3–7.9) 3 0.9 (0.3–4.4) 3 4.0 (2.1–6.4) 3 5.5 (2.9–7.4) 3 3.7 (1.4–6.0) 3 4.0 (1.2–6.7) 3 1.6 (0.3–4.9) 3 4.9 (3.1–7.6) 3 21.5±12.1 3

PSS Missing TSDS Missing

7.5 (2.6–12.4) 8 26.0±16.8 9

5.2 (2.0–9.1) 5 22.1±14.7 6

14.3 (9.6–19.8) 3 35.8±17.6 3

0.008a 0.30a <0.0001a <0.0001a 0.08a 0.01a 0.53a <0.0001a 0.009b <0.0001a <0.0001b

2800

Support Care Cancer (2012) 20:2795–2802

Table 4 Univariate and multivariate analysis for BEDS >6

a

Adjusted on age, sex, and other significant parameters from the univariate analysis

Variables

Univariate OR (95% CI)

p

Multivariatea OR (95% CI)

Pain Fatigue Nausea Anxiety Drowsiness Shortness of breath Loss of appetite Well-being

1.014 (1.00–1.03) 1.019 (1.005–1.033) 1.009 (0.996–1.023) 1.051 (1.033–1.07) 1.011 (0.998–1.024) 1.02 (1.006–1.035) 1.002 (0.989–1.015) 1.032 (1.017–1.048)

0.06 0.007 0.18 <0.0001 0.09 0.005 0.78 <0.0001

– 0.998 (0.978–1.018) – 1.052 (1.028–1.077) – 0.996 (0.973–1.019) – 1.011 (0.989-1.033)

BEDS score >6 receiving antidepressants. Furthermore, there was no reference in our patients' medical charts to the presence of depression or that they were receiving nonpharmacological treatment such as counseling or cognitive behavioral therapy. The other important finding was the significant and consistent association between the probable presence of depression as determined with the BEDS and the symptom distress detected in the ESAS. The ESAS items associated with probable depression included both psychological symptoms (depression, anxiety, feeling of well-being), and somatic symptoms (fatigue, shortness of breath). Fatigue has previously been reported to be more frequent and severe among depressed than nondepressed patients [15, 42, 43]. Our finding suggests that depression is more common in patients who report much higher level of fatigue in ESAS. This is not possible to establish if fatigue is the reason why patients became depressed, or if due to depression patients express fatigue at a higher level. More research is necessary to determine the nature of this association, and this will likely include long-term follow-up. A previous study reported the association of depression and shortness of breath, and one of the explanations might be that patients with higher intensity of dyspnea are patients with more advanced stage of malignancy [18]. We were expecting to find a strong association between pain and depression as previously reported in many studies, but in our sample, there was no significant association between these two symptoms [15, 44]. This can be partially explained by the overall low intensity of pain in our sample Table 5 ESAS item score sensitivity and specificity to BEDS Different cutoff Depression Depression Depression Depression

≥1 ≥2 ≥3 ≥4

Sensitivity

Specificity

PPV

NPV

0.88 0.73 0.53 0.43

0.57 0.74 0.88 0.97

0.54 0.62 0.71 0.88

0.89 0.83 0.76 0.75

ESAS Edmonton Symptom Assessment System, PPV positive predictive value, NPV negative predictive value

p

0.83 <0.0001 0.71 0.34

(the median score of ESAS item for pain was 2). Our clinical finding strongly suggests that when patients express high intensity of symptoms such fatigue, careful screening for depression is indicated. Because the ESAS items of depression, anxiety, and feeling of well-being as well as the overall psychosocial score were significantly associated with probable depression as determined with the BEDS, information on these ESAS items will likely allow for appropriate screening for depression. Thus, an ESAS score of ≥2 (out of a possible 10) for depression item would justify further assessment. In an earlier study, Vignaroli et al. [28] also determined that an ESAS score of ≥2 was optimal as a screening tool. In other words, the BEDS does not need to be used for systematic screening; appropriate screening can be achieved with regular use of the ESAS in the clinical setting. We found that a previous history of depression is a major predictor of being depressed, as is well known in the literature for the general population (http://www.psych.org/ guidelines/mdd2010). Therefore, any patient with a history of depression should be screened, not only at the moment of cancer diagnosis but throughout the trajectory of the illness. Weaknesses of this study include the fact that we used a screening tool to assess depression rather than the gold standard. Indeed, all the screening tools will miss real cases (false negative) and identify wrong cases (false positive), then comparing a screening tool to other screening tools might lead to limited conclusions as the gold standard used did not have an excellent accuracy. There are a number of excellent tools for the screening of depression, including the PHQ-9 [45, 46], CES-D [47, 48], HADS [49–51], and BDI [52] as examples. Most of these tools would have been an appropriate gold standard for the comparison with the ESAS. We chose BEDS since it has been validated for patients with advanced cancer showing a good reliability and validity [31]. Furthermore, in the validation study, the BEDS was better able than the 10-item EDS, from which it was derived, to discriminate between cases and noncases of depression as identified by an interview using the Present State Examination (a semi structured

Support Care Cancer (2012) 20:2795–2802

psychiatric interview based on establishing symptoms and degree of severity) [31]. Thus, we assume that although the ESAS is just a screening tool, it still gives us a real picture of the frequency of depression and of its associated symptoms. The other main limitation of the study is the cross-sectional design that did not allow us to know how the frequency of depression changes over the time. More research is necessary not only on the screening for and detection of depression but also on pharmacological and nonpharmacological interventions for cancer-related depression. Both pharmacological and nonpharmacological approaches can be effective for the management of depression. For example, palliative care consultation has been shown to significantly improve the ESAS depression score even after a single visit [53]. Temel et al. [54] found that cancer patients seen early for a palliative care consultation experienced significant improvement in their depression level and lived longer. Thus, the assessment for and appropriate management of depression can not only significantly affect the quality of life but also, as has been shown for cardiovascular disease and others chronic conditions, prolong life. Despite available treatments and the improvement of the awareness of the clinicians taking care of cancer patients, depression remains under-diagnosed and thus under-treated. Therefore, depression assessment necessitates systematic screening with adapted tools like the ESAS. There is also a need to improve the documentation on the screening and the orientation proposed to patients, because depression screening can be efficient only if oncologists have the training and the resources to confirm depression diagnosis and to propose effective treatment. It is important that efforts to improve detection of depression are accompanied by efforts to improve treatment as well [55]. More research is necessary to confirm our preliminary findings.

Acknowledgment This research is supported by a grant from the Apicil Foundation. Conflicts of interest None.

References 1. Trask PC (2004) Assessment of depression in cancer patients. J Natl Cancer Inst Monogr 32:80–92 2. Hotopf M, Chidgey J, Addington-Hall J, Ly KL (2002) Depression in advanced disease: a systematic review. Part 1. Prevalence and case finding. Palliat Med 16:81–97 3. Meyer HA, Sinnott C, Seed PT (2003) Depressive symptoms in advanced cancer. Part 1. Assessing depression: the mood evaluation questionnaire. Palliat Med 17:596–603

2801 4. Reeve JL, Lloyd-Williams M, Dowrick C (2008) Revisiting depression in palliative care settings: the need to focus on clinical utility over validity. Palliat Med 22:383–391 5. Mitchell AJ, Chan M, Bhatti H, Halton M, Grassi L, Johansen C, Meader N (2011) Prevalence of depression, anxiety, and adjustment disorder in oncological, haematological, and palliative-care settings: a meta-analysis of 94 interview-based studies. Lancet Oncol 12:160–174 6. Passik SD, Dugan W, McDonald MV, Rosenfeld B, Theobald DE, Edgerton S (1998) Oncologists' recognition of depression in their patients with cancer. J Clin Oncol 16:1594–1600 7. Fallowfield L, Ratcliffe D, Jenkins V, Saul J (2001) Psychiatric morbidity and its recognition by doctors in patients with cancer. Br J Cancer 84:1011–1015 8. Lawrie I, Lloyd-Williams M, Taylor F (2004) How do palliative medicine physicians assess and manage depression. Palliat Med 18:234–238 9. Breitbart W (1995) Identifying patients at risk for, and treatment of major psychiatric complications of cancer. Support Care Cancer 3:45–60 10. Uitterhoeve RJ, Vernooy M, Litjens M, Potting K, Bensing J, De Mulder P, van Achterberg T (2004) Psychosocial interventions for patients with advanced cancer—a systematic review of the literature. Br J Cancer 91:1050–1062 11. Rodin G, Lloyd N, Katz M, Green E, Mackay JA, Wong RK (2007) The treatment of depression in cancer patients: a systematic review. Support Care Cancer 15:123–136 12. Rayner L, Price A, Evans A, Valsraj K, Hotopf M, Higginson IJ (2011) Antidepressants for the treatment of depression in palliative care: systematic review and meta-analysis. Palliat Med 25:36–51 13. Stiefel R, Die Trill M, Berney A, Olarte JM, Razavi A (2001) Depression in palliative care: a pragmatic report from the Expert Working Group of the European Association for Palliative Care. Support Care Cancer 9:477–488 14. Jacobsen PB, Shibata D, Siegel EM, Lee JH, Fulp WJ, Alemany C, Abesada-Terk G, Jr, Brown R, Cartwright T, Faig D, Kim G, Levine R, Markham MJ, Schreiber F, Sharp P, Malafa M (2011) Evaluating the quality of psychosocial care in outpatient medical oncology settings using performance indicators. Psychooncology 20(11):1221–1227 15. Lloyd-Williams M, Dennis M, Taylor F (2004) A prospective study to determine the association between physical symptoms and depression in patients with advanced cancer. Palliat Med 18:558–563 16. Laird BJ, Boyd AC, Colvin LA, Fallon MT (2009) Are cancer pain and depression interdependent? A systematic review. Psychooncology 18:459–464 17. Lo C, Zimmermann C, Rydall A, Walsh A, Jones JM, Moore MJ, Shepherd FA, Gagliese L, Rodin G (2010) Longitudinal study of depressive symptoms in patients with metastatic gastrointestinal and lung cancer. J Clin Oncol 28:3084–3089 18. Salvo N, Zeng L, Zhang L, Leung M, Khan L, Presutti R, Nguyen J, Holden L, Culleton S, Chow E (2012) Frequency of reporting and predictive factors for anxiety and depression in patients with advanced cancer. Clin Oncol (R Coll Radiol) 24(2):139–148 19. DiMatteo MR, Lepper HS, Croghan TW (2000) Depression is a risk factor for noncompliance with medical treatment: metaanalysis of the effects of anxiety and depression on patient adherence. Arch Intern Med 160:2101–2107 20. Pelletier G, Verhoef MJ, Khatri N, Hagen N (2002) Quality of life in brain tumor patients: the relative contributions of depression, fatigue, emotional distress, and existential issues. J Neurooncol 57:41–49 21. Cukor D, Rosenthal DS, Jindal RM, Brown CD, Kimmel PL (2009) Depression is an important contributor to low medication adherence in hemodialyzed patients and transplant recipients. Kidney Int 75:1223–1229

2802 22. Holland JC, Alici Y (2010) Management of distress in cancer patients. J Support Oncol 8:4–12 23. Satin JR, Linden W, Phillips MJ (2009) Depression as a predictor of disease progression and mortality in cancer patients: a metaanalysis. Cancer 115:5349–5361 24. Lloyd-Williams M, Shiels C, Taylor F, Dennis M (2009) Depression—an independent predictor of early death in patients with advanced cancer. J Affect Disord 113:127–132 25. Mitchell AJ, Kaar S, Coggan C, Herdman J (2008) Acceptability of common screening methods used to detect distress and related mood disorders—preferences of cancer specialists and nonspecialists. Psychooncology 17:226–236 26. Rhondali W, Perceau E, Blay JY, Fournel-Federico C, Saltel P, Trillet-Lenoir V, Tredan O, Coulon JP, Bruera E, Filbet M (2012) Depression assessment by oncologists and palliative care physicians. Palliat Support Care 10(4), in press 27. Lees N, Lloyd-Williams M (1999) Assessing depression in palliative care patients using the visual analogue scale: a pilot study. Eur J Cancer Care (Engl) 8:220–223 28. Vignaroli E, Pace EA, Willey J, Palmer JL, Zhang T, Bruera E (2006) The Edmonton Symptom Assessment System as a screening tool for depression and anxiety. J Palliat Med 9:296–303 29. Wasteson E, Brenne E, Higginson IJ, Hotopf M, Lloyd-Williams M, Kaasa S, Loge JH (2009) Depression assessment and classification in palliative cancer patients: a systematic literature review. Palliat Med 23:739–753 30. Dugan W, McDonald MV, Passik SD, Rosenfeld BD, Theobald D, Edgerton S (1998) Use of the Zung Self-Rating Depression Scale in cancer patients: feasibility as a screening tool. Psychooncology 7:483–493 31. Lloyd-Williams M, Shiels C, Dowrick C (2007) The development of the Brief Edinburgh Depression Scale (BEDS) to screen for depression in patients with advanced cancer. J Affect Disord 99:259–264 32. Rhondali W, Perceau E, Saltel P, Girard R, Filbet M (2011) Translation and validation of Brief Edinburgh Depression Scale (BEDS) in French. Bull Cancer 98:199–208 33. Oken MM, Creech RH, Tormey DC, Horton J, Davis TE, McFadden ET, Carbone PP (1982) Toxicity and response criteria of the Eastern Cooperative Oncology Group. Am J Clin Oncol 5:649–655 34. Cummings G, Biondo PD, Campbell D, Stiles C, Fainsinger R, Muise M, Hagen N (2011) Can the global uptake of palliative care innovations be improved? Insights from a bibliometric analysis of the edmonton symptom assessment system. Palliat Med 25:71–82 35. Bruera E, Kuehn N, Miller MJ, Selmser P, Macmillan K (1991) The Edmonton Symptom Assessment System (ESAS): a simple method for the assessment of palliative care patients. J Palliat Care 7:6–9 36. Chang VT, Hwang SS, Feuerman M (2000) Validation of the Edmonton Symptom Assessment Scale. Cancer 88:2164–2171 37. Richardson LA, Jones GW (2009) A review of the reliability and validity of the Edmonton Symptom Assessment System. Curr Oncol 16:55 38. Bruera E, MacMillan K, Hanson J, MacDonald RN (1989) The Edmonton staging system for cancer pain: preliminary report. Pain 37:203–209 39. Cheung WY, Barmala N, Zarinehbaf S, Rodin G, Le LW, Zimmermann C (2009) The association of physical and psychological symptom burden with time to death among palliative cancer outpatients. J Pain Symptom Manage 37:297–304 40. Moro C, Brunelli C, Miccinesi G, Fallai M, Morino P, Piazza M, Labianca R, Ripamonti C (2006) Edmonton symptom assessment

Support Care Cancer (2012) 20:2795–2802

41.

42.

43.

44.

45.

46.

47.

48.

49.

50.

51.

52.

53.

54.

55.

scale: Italian validation in two palliative care settings. Support Care Cancer 14:30–37 Carvajal A, Centeno C, Watson R, Bruera E (2011) A comprehensive study of psychometric properties of the Edmonton Symptom Assessment System (ESAS) in Spanish advanced cancer patients. Eur J Cancer 47:1863–1872 Zeng L, Koo K, Zhang L, Jon F, Dennis K, Holden L, Nguyen J, Tsao M, Barnes E, Danjoux C, Sahgal A, Chow E (2011) Fatigue in advanced cancer patients attending an outpatient palliative radiotherapy clinic as screened by the Edmonton Symptom Assessment System. Support Care Cancer Kroenke K, Zhong X, Theobald D, Wu J, Tu W, Carpenter JS (2010) Somatic symptoms in patients with cancer experiencing pain or depression: prevalence, disability, and health care use. Arch Intern Med 170:1686–1694 Laird BJ, Scott AC, Colvin LA, McKeon AL, Murray GD, Fearon KC, Fallon MT (2011) Pain, depression, and fatigue as a symptom cluster in advanced cancer. J Pain Symptom Manage 42:1–11 Kroenke K, Spitzer RL, Williams JB (2001) The PHQ-9: validity of a brief depression severity measure. J Gen Intern Med 16:606– 613 Thekkumpurath P, Walker J, Butcher I, Hodges L, Kleiboer A, O'Connor M, Wall L, Murray G, Kroenke K, Sharpe M. Screening for major depression in cancer outpatients: the diagnostic accuracy of the 9-item patient health questionnaire. Cancer 117(1):218–227 Schroevers MJ, Sanderman R, van Sonderen E, Ranchor AV (2000) The evaluation of the Center for Epidemiologic Studies Depression (CES-D) scale: depressed and positive affect in cancer patients and healthy reference subjects. Qual Life Res 9:1015– 1029 Hann D, Winter K, Jacobsen P (1999) Measurement of depressive symptoms in cancer patients: evaluation of the Center for Epidemiological Studies Depression Scale (CES-D). J Psychosom Res 46:437–443 Luckett T, Butow PN, King MT, Oguchi M, Heading G, Hackl NA, Rankin N, Price MA (2010) A review and recommendations for optimal outcome measures of anxiety, depression and general distress in studies evaluating psychosocial interventions for English-speaking adults with heterogeneous cancer diagnoses. Support Care Cancer 18:1241–1262 Mitchell AJ (2010) Short screening tools for cancer-related distress: a review and diagnostic validity meta-analysis. J Natl Compr Canc Netw 8:487–494 Johnston M, Pollard B, Hennessey P (2000) Construct validation of the hospital anxiety and depression scale with clinical populations. J Psychosom Res 48:579–584 Berard RM, Boermeester F, Viljoen G (1998) Depressive disorders in an out-patient oncology setting: prevalence, assessment, and management. Psychooncology 7:112–120 Yennurajalingam S, Urbauer DL, Casper KL, Reyes-Gibby CC, Chacko R, Poulter V, Bruera E (2010) Impact of a palliative care consultation team on cancer-related symptoms in advanced cancer patients referred to an outpatient supportive care clinic. J Pain Symptom Manage. doi:10.1016/j.jpainsymman.2010.03.017 Temel JS, Greer JA, Muzikansky A, Gallagher ER, Admane S, Jackson VA, Dahlin CM, Blinderman CD, Jacobsen J, Pirl WF, Billings JA, Lynch TJ (2010) Early palliative care for patients with metastatic non-small-cell lung cancer. N Engl J Med 363:733–742 Hotopf M (2008) Review: screening or case-finding questionnaires used alone are not effective in the management of depression. ACP J Club 149:9