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Original article

Predicting depression with temperament and character in lung cancer patients B. AUKST MARGETIC´, MD, PHD, Department of Psychiatry, University Hospital Center Zagreb, Zagreb, S. KUKULJ, MD, PHD, ASSOCIATE PROFESSOR, Department of Pulmonary Diseases Jordanovac, University Hospital Center Zagreb, Zagreb, Croatia, Ž. ŠANTIC´, MD, PHD, PROFESSOR, University School of Medicine Mostar, Mostar, Bosnia and ´ , MS, Department of Psychiatry, University Hospital Center Zagreb, Zagreb, & Herzegovina, N. JAKŠIC ´ M. JAKOVLJEVIC, MD, PHD, PROFESSOR, Department of Psychiatry, University Hospital Center Zagreb, Zagreb, Croatia ´ Ž., JAKŠIC ´ N. & JAKOVLJEVIC´ M. (2013) European Journal of AUKST MARGETIC´ B., KUKULJ S., ŠANTIC Cancer Care 22, 807–814 Predicting depression with temperament and character in lung cancer patients Depression is highly prevalent in cancer patients. Variations in intensity and frequency of depression in cancer patients may be attributed, in part, to differences in personality dimensions. Our aim was to asses if dimensions of temperament and character could predict depression in lung cancer patients. Ninety newly diagnosed non-small cell lung cancer patients were assessed in the oncology unit with the Centre for Epidemiologic Studies Depression Scale (CES-D), pain subscale of the European Organization for Research and Treatment of Cancer Quality of Life Questionnaire (EORTC QLQ) C30 and the Temperament and Character Inventory (TCI). Fifty out of 90 patients (55.6%) fulfilled the cut-off criteria for depression on the CES-D scale. Logistic regression performed to assess if depression was predicted by personality dimensions, revealed dimension of temperament Harm Avoidance and pain as significant predictors of depression. Depressive reactions are highly prevalent in lung cancer patients and related to patients’ personality. These findings may be helpful in planning preventive, as well as psychoeducational and treatment programmes for newly diagnosed, and depression prone patients.

Keywords: depression, lung cancer, oncology patients, personality, temperament.

INTRODUCTION Due to the life-threatening illness and severe side effects of treatment, depression is common in oncological patients during the clinical course of the disease. The prevalence rates of clinical depression and its subsyndromal symptoms in cancer patients have been reported to range from 10% to more than 50% (Carlsen et al. 2005). Correspondence address: Branka Aukst Margetic, Department of Psychiatry, University Hospital Center Zagreb, Kišpatic´eva 12, 10000 Zagreb, Croatia (e-mail: [email protected]). There was no external funding or support in preparing this manuscript.

Accepted 26 April 2013 DOI: 10.1111/ecc.12080 European Journal of Cancer Care, 2013, 22, 807–814

© 2013 John Wiley & Sons Ltd

These variations in prevalence reflect, among other, differences in assessment tools, definition of depression, time passed since diagnosis, and disease sites or stages (Massie 2004; Carlsen et al. 2005; Brintzenhofe-Szoc et al. 2009; Hinz et al. 2010). Lung cancer is the most common form of cancer and is the leading cause of cancer-related deaths worldwide in male population (Jemal et al. 2011). It is still prognostically very unfavourable with an overall 5-year survival rate of only 15% (Herbst et al. 2005). Furthermore, lung cancer patients have particularly high rates of clinically significant depression (Massie 2004; Carlsen et al. 2005; Brintzenhofe-Szoc et al. 2009). As the care for lung cancer has improved and expected survival prolonged, the significance of assessment and

´ ET AL. AUKST MARGETIC

treatment of depressive states has increased. In a review of psychosocial aspects of lung cancer, it was emphasised that additional studies were needed to identify the patients particularly at risk for depressive reactions, evaluate differences in reactions to diagnosis of lung cancer, as well as intensity of depressive reactions (Carlsen et al. 2005). Patients who are newly diagnosed with cancer display a complex array of highly individual psychosocial responses. Variations in coping with cancer, and subsequently in severity and frequency of depression, are not only due to nature or severity of the illness alone (Akechi et al. 2001). They may also be attributed, at least in some part, to personality (Kalogreades & Corr 2011), defined as those characteristics of the person that account for consistent patterns of feelings, thoughts and behaviour (Aarstad et al. 2003). Personality characteristics play an important role in influencing the subjective perception of situations and the consequent reactions to them (Rossi Ferrario et al. 2003). The psychobiological model developed by Cloninger and his colleagues is based on four temperament and three character dimensions (Cloninger et al. 1993). The characterological aspects of personality involve individual differences in self-concepts about goals and values, in contrast to the temperament that involves differences in automatic emotional reactions and habits. Such self-concepts modify the significance or meaning of what is experienced, hence, also changing emotional reactions and habits. Cloninger and his colleagues identify four temperament dimensions which are considered to be biologically based and highly heritable individual differences in habits and skills: Harm Avoidance (HA), which is defined as pessimistic worrying in anticipation of problems; Novelty Seeking (NS), which describes the initiation of the appetitive approach in response to novelty; Reward Dependence (RD) which describes the maintenance of the behaviour in response to cues of social reward and Persistence (P), which is defined as perseverance despite frustration and fatigue (Cloninger et al. 1993). Accordingly, the three character dimensions include both an intellectual perspective about self/non-self boundaries and an emotional perspective and may be crucial in stress appraisal and adjustment process. Character dimension Self-Directedness (SD) is defined as having will-power and determination, Cooperativeness (C) describes individual differences with regard to tolerance and empathy and Self-Transcendence (ST) characterises individual differences in spirituality. The character dimensions mature in response to learning and life experiences and can influence the expressions of temperament (Cloninger et al. 1993). 808

The psychobiological model has not been used so far in the assessment of cancer patients, but high Harm Avoidance and low Self-directedness show strong associations with depression in general population (Grucza et al. 2003; Cloninger et al. 2006), as well as in various clinical populations (Hansenne et al. 1999; Boz et al. 2004; Celikel et al. 2009). High Harm Avoidance reflects anxious persons prone to depression and pessimism, while low Self-Directedness reflects personality features such as responsibility, purposefulness, resourcefulness and selfacceptance (Cloninger et al. 1993; Svrakic & Cloninger 2010). Other personality models and their measures, such as Eysenck Personality Inventory (Eysenck & Eysenck 1965) and NEO Personality Inventory (Costa & McCrae 1989) were previously used in studying the associations between personality and cancer risk and survival (Hansen et al. 2005; Nakaya et al. 2005). The role of broad personality dimensions in depression prevalence among lung cancer patients has been investigated in only one very recent study (Shimizu et al. 2012). Our aim was to assess the association of temperament and character dimensions with depression in lung cancer patients. There were no external funding sources for this study.

METHODS Participants In this study 90 newly diagnosed inpatients (73.37% male) (mean age 61.1 years, SD 7.52) with non-small cell cancer were consecutively assessed in the oncology unit before starting with any treatment procedure. The interviews took place within the first week of their admission to the hospital. The results were collected during 2010 and 2011. Patients who fulfilled the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition (DSM-IV) criteria for mental retardation, organic brain disease, severe physical disorders, and those with low comprehension skills were excluded. Eleven patients of those who fulfilled inclusion criteria refused to participate; 15 failed to complete the evaluation for various reasons (poor physical state, dementia, early discharge from hospital). Nonresponders did not differ significantly from responders in gender and age. No missing data were obtained by the researchers’ visual inspection of the instruments after they were filled out by the participants. Informed consent was obtained after the aim and purpose of the study was thoroughly explained. The study was approved by the Ethical Committee of the University Hospital Centre Zagreb. © 2013 John Wiley & Sons Ltd

Depression and personality in lung cancer patients

Measures Depression was measured with the Centre for Epidemiologic Studies Depression Scale (CES-D) (Radloff 1977), a 20-item self-report scale designed to measure depressive symptoms in general community. The scale was previously used with cancer patients (Kurtz et al. 2002; Aukst-Margetic´ et al. 2005), as its use in this population is advocated instead of other depression scales that include more items focused on the effects of cancer, such as weight loss (Hann et al. 1999). Respondents indicate how often within the last week they experienced certain symptoms, responding with: ‘rarely or none of the time’ (0); ‘some or little of the time’ (1); ‘occasionally or a moderate amount of time’ (2); and ‘most or all of the time’ (3). The scores for the 20 items are added, resulting in a range of possible total scores from 0 to 60. The score of 16 and higher was taken to indicate clinically relevant depressive syndrome (Radloff 1977). Studies have reported high internal reliability of the CES-D in cancer patients (Hann et al. 1999; Kurtz et al. 2002; Aukst-Margetic´ et al. 2005). In our sample, the Cronbach’s alpha coefficient was 0.89. For measuring physical pain, as one of the main predictors of depression in cancer patients (Massie 2004; Wong et al. 2010), we used a subscale from the European Organization for Research and Treatment of Cancer Quality of Life Questionnaire (EORTC QLQ-C30; European Organization for Research and Treatment of Cancer 2001), which is one of the most widely used measures of cancer-related quality of life (QoL). It is a 30-item instrument measuring level of functioning (LoF), symptom severity (SS), and quality of life (QoL). The Croatian version of EORTC QOL-C30 was developed following rigorous EORTC translation procedures and has been validated in previous research (Pinjatela 2008). The pain subscale is one of the symptom scales with a range from 0 to 100 where higher scores indicate higher perception of pain. Personality was assessed using the Croatian adaptation of the Temperament and Character Inventory (TCI) (Cloninger et al. 1993). The TCI is a self-report questionnaire consisting of 240 items requiring a true/false response. The translation of the American original into Croatian language was carried out following the guidelines developed by the World Health Organization (Sartorius & Kuyken 1994). The instrument was previously validated in a domestic sample of 360 persons and showed good reliability (Aukst Margetic´ et al. 2011a). The Cronbach’s alpha coefficients of the TCI dimensions in this sample were: Novelty Seeking (0.55), Harm Avoidance (0.74), Reward Dependence (0.48), Persistence (0.44), © 2013 John Wiley & Sons Ltd

Self-Directedness (0.78), Cooperativeness (0.54) and SelfTranscendence (0.78). Only the main scores of the four temperament and three character dimensions of the TCI were reported in this study. Disease severity was determined by the cancer stage (American Joint Committee on Cancer 1992), a measure of tumour size and metastases based on TNM (tumour-nodemetastasis) classification (Goldstraw 2009). Forty-four point four per cent (44.4%) of the patients were diagnosed with stage IV, 40.0% with stage III and 15.6% with stage I/II lung cancer. Statistical analyses Statistical analyses were performed using the spss 16.0 statistical package. Standard descriptive statistics including means, standard deviations, frequency counts, percentages, as well as internal consistency coefficients were calculated. The Kolmogorov–Smirnov test was applied for assessing whether the distribution of continuous variables was normal. Based on the cut-off score on the CES-D scale, patients were categorised into two groups. The t-test and the Mann–Whitney test were used for comparisons of continuous and the chi-squared test for comparisons of categorical variables. The Bonferroni correction was performed for multiple comparisons made with the t-test. The logistic regression was performed to assess if personality dimensions were predictors of depression in newly diagnosed lung cancer patients. In order to control for the influence of age, gender, tumour grade and physical pain, these variables were entered into the analysis in the first block. The temperament and character dimensions, as exploratory predictor variables, were entered into the second block. RESULTS Mean score for depression was 18.24 (SD 10.23). Fifty out of 90 patients (55.6%) fulfilled the cut-off criteria for depression. The mean pain perception was 28.14 (SD 28.44). Means and standard deviations of temperament and character dimension were: NS 16.32 (4.23); HA 16.23 (5.19); RD 13.9 (2.84); P 2.95 (1.35) SD 29.6 (6.28); C 30.34 (3.59); ST 16.63 (5.28). There were no differences between the depressed and non-depressed patients based on gender, age and tumour grade, but patients differed based on the level of pain (t = 2.778; d.f. = 88; P = 0.007) as well as temperament dimension Harm Avoidance (t = 3.581; d.f. = 88; P = 0.001) after using the Bonferroni corrections for multiple comparisons. Depressed patients felt more pain and had higher scores on temperament dimension Harm Avoidance. 809


Table 1. Results of the logistic regression analysis of personality dimensions as predictors of depression while controlling for the influence of age, gender, tumour grade and physical pain Gender Age Grade I/II Grade III Grade IV Pain NS HA RD P SD C ST

B

WALD

P

Exp(B)

CI 95% for exp(B)

-0.321 -0.058

0.261 2.414 3.981 0.044 3.290 3.889 0.938 5.290 0.000 0.057 1.183 0.914 0.797

0.609 0.120 0.137 0.833 0.070 0.049 0.333 0.021 0.989 0.811 0.277 0.339 0.372

0.726 0.944

0.212–2.481 0.878–1.015

1.206 0.354 1.020 0.940 1.174 1.001 1.052 0.940 1.079 0.947

0.211–6.894 0.115–1.087 1.000–1.040 0.828–1.066 1.024–1.346 0.832–1.206 0.695–1.591 0.841–1.051 0.923–1.261 0.839–1.068

0.187 -1.038 0.020 -0.062 0.160 0.001 0.050 -0.062 0.076 -0.055

C, Cooperativeness; HA, Harm Avoidance; NS, Novelty Seeking; RD, Reward Dependence; P, Persistence; SD, Self-Directedness; ST, Self-Transcendence; WALD, Wald statistic. Statistically significant values are highlighted in bold.

Logistic regression was performed to assess if depression was predicted by personality dimensions controlling for age, gender, tumour stage and pain (Table 1). The analyses revealed temperament dimension Harm Avoidance and physical pain as unique predictors of depression in patients with lung cancer.

DISCUSSION Depression in lung cancer patients was shown to be uniquely predicted by temperament dimension Harm Avoidance and level of physical pain. Most studies assessing depression prevalence have included cancer stage, histological type, gender, age, marital status, performance status, co-morbidity, physical symptoms and socioeconomic background as confounding factors (Shimizu et al. 2012). Most of these factors were controlled for in our analysis. The psychological correlates of depressive symptoms in lung cancer patients, such as personality dimensions and personality related concepts like coping strategies (Walker et al. 2006) and perceived stigma (Gonzalez & Jacobsen 2012), have been studied to a much lesser extent. Self-attribution and self-efficacy may have a critical role in the actual level of distress and psychological adjustment in patients with lung cancer (Faller et al. 1995). Well-known associations with smoking as a causal factor could lead to self-rapprochement and self-criticism (LoConte et al. 2008), as well as shame and perceived stigma (Chapple et al. 2004). Such self-evaluating constructs are known to be dependent on patients’ personality (Hernández et al. 2007; Aukst Margetic´ et al. 2010) and have shown positive correlations with Neuroticism in several studies (Rossi Ferrario et al. 2003; van der Steeg 810

et al. 2007). The construct of Neuroticism and trait anxiety have also been investigated in cancer patients and linked to cancer risk and survival (Weihs et al. 2000; Hansen et al. 2005; Nakaya et al. 2005) and long-term quality of life (Härtl et al. 2010). Furthermore, greater risk for depression was strongly associated with Neuroticism in the only study that focused on the role of broad personality in depression prevalence among lung cancer patients (Shimizu et al. 2012). Cloninger’s model of personality has not so far been used in cancer populations. Harm Avoidance, a temperament dimension rather similar to Neuroticism (Masthoff et al. 2007), is characterised by proneness to being passive, insecure, pessimistic, tense and anxious in situations that usually do not worry other people (Cloninger et al. 1993). Higher Harm Avoidance was shown to be the risk factor for depression in various populations (Hansenne et al. 1999; Boz et al. 2004; Celikel et al. 2009) and was increased even when patients were in the euthymic phase of the disease (Cloninger et al. 2006). Because personality is thought to be a relatively stable concept, lung cancer patients high on Harm Avoidance should be regarded as having an increased risk for developing depression. Assessing symptoms of depression and personality dimensions in newly diagnosed patients has special importance as depression and anxiety might be the first symptoms of lung cancer (Spiegel & Giese-Davis 2003; Carlsen et al. 2005). It is not without importance to notice that it is unlikely in cancer patients with higher Harm Avoidance to use denial, a defence mechanism that has been associated with less depression and anxiety (Vos et al. 2011) and better health-related quality of life (Paika et al. 2010) among these patients. Although the general level of pain in our sample was in the lower third, it was the only disease-related variable © 2013 John Wiley & Sons Ltd


that predicted depression. The correlations between pain and depression are known from many studies with different cancer sites (Laird et al. 2009), while cause–effect relationship between depression and pain is still not completely clear. Pain is one of the most common symptoms of lung cancer (Krech et al. 1992; Cooley 2000) and is a major concern of patients with other types of cancer as well. Cancer patients who are experiencing pain are much more likely to have high levels of depression and anxiety, lower quality of life and other cancer symptoms such as fatigue, dyspnoea, loss of appetite, coughing and insomnia (Glover et al. 1995; Tavoli et al. 2008; Laird et al. 2009). Perception of pain can create a sense of hopelessness, because patients fear that their lives are not worth continuing or they lose the meaning of life if they must feel continuous pain (Tavoli et al. 2008). The study showed high prevalence of depression in lung cancer patients, somewhat higher but still comparable to most other studies reporting clinically significant depressive symptoms shortly after diagnosis (Buccheri 1998; Montazeri et al. 1998; Hopwood & Stephens 2000; Turner et al. 2007; Rolke et al. 2008). Self-report instruments generally show higher depression rates in comparison to structured psychiatric interviews (Carlsen et al. 2005). Self-report measures of depression like CES-D are screening instruments that actually measure depressive reactions in the situation of newly diagnosed life-threatening disease. Furthermore, a somewhat lower but widely used cut-off score of ⱖ16 (Radloff 1977; Katz et al. 2004; Gonzalez & Jacobsen 2012) was applied in this study, which could partly account for an increased number of depressed cancer patients. Due to the life-threatening illness and various severe side effects of treatment, the fact that depression is common in oncological patients is of no surprise. Besides, lung cancer carries a rather poor prognosis, as the disease is often diagnosed in the later stages (Massie 2004). Adjustment to cancer is a process of many peaks of depression and anxiety and the time shortly after diagnosis is especially stressful (Ballenger et al. 2001). Psychological reactions are generally under-investigated in lung cancer patients and the knowledge of general level of depression is relevant, because prospective studies have reported a significant association of clinical depression and its subsyndromal symptoms with cancer mortality (Hjerl et al. 2003; Goodwin et al. 2004), even after controlling for confounding medical variables (Pinquart & Duberstein 2010). Furthermore, depression represents one of the most significant risk factors for suicidal ideation and completed suicide in cancer patients (Robson et al. 2010; Kalogreades & Corr 2011). Accordingly, screening © 2013 John Wiley & Sons Ltd

for depression as well as implementing strategies targeting patients high on certain personality dimensions should be used in the oncological settings and discussed within the multidisciplinary teams of experts. Supportive relationship with the oncology team members is highly valued by the patients (Salander & Henriksson 2005; Gilbert et al. 2011) and associated with better quality of life (Teutsch 2003). Besides, introducing oncologists about patients’ well-being including anxiety and depression levels has shown the potential to improve patients’ symptom control (Boyes et al. 2006). Personality research and assessment has important implications for the prevention and treatment of depression. Personality traits can be assessed relatively easily and efficiently (e.g. by using the short form of the TCI for screening purposes) and may point to at risk individuals who could benefit from prevention of depressive disorders (Kovacs & Lopez-Duran 2010). Furthermore, psychobiological model allows comprehensive description of patient’s personality and accordingly may help in treatment decisions (Conrad et al. 2007). Substantial evidence has accumulated indicating that antidepressant treatment decreases temperament dimension Harm Avoidance, while individuals with higher scores on Harm Avoidance show poorer treatment response (Kampman & Poutanen 2011), including interpersonal psychotherapy and cognitive-behavioural therapy (Joyce et al. 2007), as well as treatment with antidepressants (Kampman et al. 2012). The studies have also shown that cognitive-behavioural therapy increases Self-Directedness (Anderson et al. 2002) and that higher Self-Directedness may predict better response to cognitive-behavioural therapy (Bulik et al. 2000). Moreover, personality may be useful in matching patients to interventions, including choice of therapeutic strategies, the focus of therapeutic interventions, and the ways in which patients regard their treatment (Zinbarg et al. 2008). For example, Bagby et al. (2008) reported that patients high on Neuroticism (personality dimension similar to Harm Avoidance) respond better to antidepressant medication than to psychotherapy. With regard to psychosocial interventions in cancer patients, a growing body of evidence supports their usefulness for improving cancer patients’ overall quality of life (Rehse & Pukrop 2003). Recent comprehensive reviews and meta-analytical studies (Akechi et al. 2008; Li et al. 2012) have concluded that psychosocial and pharmacological interventions have been shown to be efficacious in treating depression in cancer, even in advanced stages of the disease. More specifically, individual or group cognitive-behavioural, psychoeducational and supportive interventions and pharmacotherapy, as well as their different combinations, 811


have been recommended in the population of cancer patients (Jacobsen & Jim 2008). Despite this, more research is needed to establish the relative and combined benefit from those treatments, as well as to determine which type of treatment would be the most beneficial for patients high in Harm Avoidance. More focus needs to be put on the development and evaluation of novel interventions targeted to specific biologic and psychosocial risk factors, including personality vulnerability to depression. However, patients with lung cancer express high proportion of unmet psychological needs (Sanders et al. 2010), but due to predominance of male gender and symptoms like breathlessness, associated with advanced stages (Larsson et al. 2012), may be less prone to engage in psychotherapy. Further, these interventions are far less researched and especially out of proportion to the rates at which lung cancer affects general population in comparison to some other cancer sites (Jack et al. 2010). Finally, future studies should investigate the usefulness of the TCI in planning and predicting the outcome of psychosocial interventions in this population. For example, higher dimension Novelty Seeking has been associated with poor adherence to psychiatric treatment, which is also important in treatment type decision making (Aukst Margetic´ et al. 2011b). Limitations This study has several limitations including a relatively small sample as well as a cross-sectional design which does not allow us to be completely certain that depression assessed in patients appeared as a reaction to the lifethreatening disease. Also, there is a risk for overrepresentation of depressive symptoms in newly diagnosed patients due to acute stress reaction. Usage of screening self-report

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instruments instead of structured psychiatric interview may also lead to increased prevalence of depression. Personality traits assessed after the cancer diagnosis may also have been influenced by the psychological reactions to the diagnosis. However, the study of Montazeri et al. (2000) showed no significant differences in the levels of anxiety and depression before and 3 months after the cancer diagnosis, which may support the validity of our results. Moreover, inclusion of newly diagnosed, still untreated patients escapes the well-known depressive symptomsaugmenting effect of cancer treatment (Massie 2004; Cheng & Yeung 2013). Finally, although the TCI is rather long and not very practical for everyday clinical situations, it gives us more detailed information about personality structure and proneness to distress in cancer patients. It is noteworthy to mention that recent studies (Cloninger & Zohar 2012) have begun to use the short form of the TCI, as it is less exhausting and time consuming, which is of particular importance in oncological settings. CONCLUSIONS Depression is highly prevalent in lung cancer patients. As it is associated with worse outcomes and mortality of cancer patients, screening for depression and its treatment is important and should be shared within multidisciplinary teams of experts. Personality seems to have a relevant role in depressive reactions among lung cancer patients, as higher temperament dimension Harm Avoidance shows unique positive association with depression. Our findings might contribute to more comprehensive understanding of depressive reactions in this population. Future studies are needed to investigate the usefulness of the psychobiological model of personality in treatment planning and prediction of treatment outcomes.

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