ORIGINAL ARTICLE /ARTICLE ORIGINAL
More negative emotion and symptom burden for female cancer patients
Des émotions négatives et un poids des symptômes plus importants pour les femmes atteintes de cancer
Z.-M. Niu · Y.-S. Wang · Y. Li · X.-Y. Peng · X.-Y. Cui · Y.-K. Wu · C.-S. Liang
Received: 14 June 2013; Accepted: 27 July 2013
© Springer-Verlag France 2013
AbstractBackground: Patients’well-being may be affected by the cancer diagnosis. Psychological response is part of a reaction to the news of cancer diagnosis. Little published data concerns the gender difference of psychological responses to the news of cancer diagnosis and its influence on the symptom burden. The aim of the study is to verify the hypothesis that female cancer patients have more negative emotion and symptom burden, comparing to males.
Patients and methods: Two hundred and twenty-eight can- cer patients were assessed by self-administered question- naire. Psychological response was measured by the Chinese version of Mini-Mental Adjustment to Cancer scale, and symptom burden was measured by the physical symptom distress scale from the Rotterdam Symptom Checklist. SPSS 13.0 was used.
Results: Female cancer patients got higher scores of negative emotion (P= 0.003), cognitive avoidance (P= 0.001), and symptom burden (P = 0.028) than males. Patients with degrees lower than high school got lower scores of negative emotion and cognitive avoidance. Lung cancer patients got higher scores of negative emotion and lower scores of posi- tive attitude.
Conclusion: Female cancer patients, especially those who did not go to high school and those with lung cancer, have more negative emotion and symptom burden, comparing to males. Appropriate psychological intervention for female cancer patients deserves more attention.
KeywordsCancer · Female · Psychological response · Negative emotion · Symptom burden
Résumé Contexte: Le diagnostic du cancer peut avoir un impact sur le bien-être des patients. La réaction psycholo- gique fait partie d’une réaction à l’annonce du diagnos- tic du cancer. Peu de publications abordent la différence entre les sexes en matière de réactions psychologiques à l’annonce d’un diagnostic de cancer et son influence sur la charge psychique liée aux symptômes. L’objectif de l’étude est de vérifier l’hypothèse selon laquelle les femmes atteintes d’un cancer ressentent davantage d’émotions négatives et la charge psychique liée aux symptômes, par rapport aux hommes.
Sujets et méthodes: Deux cent vingt-huit patients atteints de cancer ont été évalués à l’aide de questionnaires autoadmi- nistrés. La réaction psychologique a été mesurée par la ver- sion chinoise de l’échelle mini-MAC (Adaptation mentale au cancer) et la charge psychique liée a été déterminé par l’échelle de détresse liée aux symptômes issus de la liste de contrôle des symptômes de Rotterdam. Le logiciel SPSS 13.0 a été utilisé.
Résultats: Les patientes atteintes de cancer ont obtenu des scores plus élevés d’émotions négatives (p = 0,003), d’évitement cognitif (p = 0,001) et de charge psychique liée aux symptômes (p = 0,028) que les hommes. Les patients dont le niveau scolaire était inférieur à l’enseigne- ment secondaire ont obtenu des scores d’émotions néga- tives et d’évitement cognitif moindres. Les patients atteints d’un cancer du poumon ont obtenu des scores plus élevés d’émotions négatives et de plus faibles scores d’attitude positive.
Conclusion : Les femmes atteintes de cancer, en particulier les femmes n’ayant pas suivi d’études secondaires et les femmes atteintes d’un cancer du poumon, ressentent davan- tage d’émotions négatives et la charge psychique liée aux symptômes par rapport aux hommes. Une intervention psy- chologique appropriée pour les femmes atteintes de cancer mérite une plus grande attention.
Mots clésCancer · Femme · Réaction psychologique · Émotions négatives · Fardeau des symptômes
Z.-M. Niu (*) · Y.-S. Wang
Department of Thoracic Oncology, Cancer Center, State Key Laboratory of Biotherapy, West China Hospital, Sichuan University, Chengdu 610041, PR China
e-mail : niuzm06@126.com
Y. Li · X.-Y. Peng · X.-Y. Cui · Y.-K. Wu · C.-S. Liang West China Hospital, Sichuan University, Chengdu 610041, PR China
DOI 10.1007/s11839-013-0431-5
Introduction
The global burden of cancer has increased largely in recent years. About 12.7 million cancer cases are estimated to have occurred in 2008 world-wide, with 56% of the cases in the economically developing world [11]. Important aspects of a patient’s well-being may be adversely affected by the diagnosis of cancer [4,16,21]. Yet in the field of cancer, reports of clinical trials are often limited to the impact of toxicity, treatment on survival, or physical symptoms, rather than inclusive of psychological responses such as negative emotion [16].
Psychological response may obviously be part of a reac- tion to the news of cancer diagnosis; in many patients it will persist, affecting the general management and symptom con- trol [16]. It is well documented that patients themselves do not disclose their emotion unless asked, and doctors were primarily influenced by patients’ outward signs, which may be misleading, and seriously underestimated negative emotion, although the importance of psychological function- ing had been emphasized [12,24,29]. A direct consequence of the underrecognition of that is its undertreatment, particu- larly when mood disorder can be deemed understandable [4,16].
There have been many suggestions of a role for psycho- logical response in the outcome of cancer [15,18,22,30].
And studies have given good general evidence that depres- sion is a significant problem in cancer patients [19,25,26].
Despite a large number of patients with cancer who receive treatment, there is little published data concerning the gender difference of psychological responses to the news of cancer diagnosis and its influence on the symptom burden. In our study, we made the hypothesis that female cancer patients have more negative emotion and symptom burden, compar- ing to males.
The aim of the study is to verify the hypothesis. We used the Chinese version of Mini-Mental Adjustment to Cancer (Mini-MAC) scale [14] data set to test the patients’psycho- logical responses; explored the association between them and age, educational background, clinical stage, and tumor site; and recorded the symptom burden for each. Our results confirmed the hypothesis.
Methods Participants
The clinical records and psychological and symptomatic data of 228 consecutive patients were retrieved from Febru- ary to June in 2012 from the department of Medical Oncol- ogy and Cancer Center, West China Hospital, Sichuan Uni- versity, China. Eligibility criteria for our study were: age
between 20 and 80 years; diagnosis 1–3 months before the inclusion date; clinical stage II~IIIa; awareness of their cancer diagnosis; no apparent serious intellectual and func- tional impairment; be in a similar economic state, not bad nor good; and receiving primary chemotherapy treatment.
This study was approved by the Ethical Committee of Sich- uan University, and written informed consent was obtained from all participants.
All patients meeting the eligibility criteria were identified from hospital records, and most of them approached during the normal hospital in-patient visits, when they were asked if they would be willing to take part in this study assessing the psychological impact of cancer. Of the eligible, 18 patients (18/260, 6.9%) refused to take part in, and 14 (14/260, 5.4%) did not finish the questionnaire. Finally, 228 cancer patients agreed to participate in the psychological assessment, and they were divided into two groups: male group and female group.
Procedure
Patients were assessed by self-administered questionnaire and they completed the study measures at 1–3 months after diagnosis.
The Chinese version of the Mini-MAC scale was used to measure the psychological response to the news of diagnosis in our study. It is a 29-item self-report measurement tool designed for use in patient settings to assess psychological response to cancer, and it concludes Negative Emotion, Positive Attitude, and Cognitive Avoidance.
The physical symptom distress scale from the Rotterdam Symptom Checklist (RSCL) [8] was used to reflect the num- ber and diversity of symptoms in cancer patients at presenta- tion. In our study, this scale was used to evaluate the symp- tom burden of the cancer patients who were receiving their primary chemotherapy treatments.
Patients’symptom experience of both psychological and physical ranged from “not at all”to “very much.” Scores given in the Mini-MAC scale and the physical symptom dis- tress scale are 0 (not at all), 1 (a little), 2 (quite a bit), and 3 (very much). The higher the score, the higher is the level of psychological response or symptom burden.
Statistical methods
T-Test was used to compare the age, psychological response, clinical stage, tumor site, and symptom burden between groups. Crosstabs were used to test the family history. For the possible predictor variable education, One-Way AVOVA was used. The statistical software we used was SPSS13.0.
We indicated a significant result withp< 0.05.
Result
The detailed information of all participants is documented in Table 1. There were no statistically significant differences at baseline between males and females relative to mean age, education, clinical stage, tumor site, and family history (all thepvalue were > 0.05).
Psychological response to cancer
We compared the psychological responses to cancer between males and females; the scores for them are listed in Table 2.
A significantly higher score of negative emotion was found for female patients than that for male patients, for whom the p value was less than 0.05 (Table 2). And the scores of posi- tive attitude of females were significantly lower than that of males. All cancer patients expressed various degree of avoidance, but there was no statistical significance between groups.
Gender might just play an important role in the psycho- logical responses of cancer patients. In order to demonstrate this, the influence of some probable factors must be taken into consideration.
Probable factors associated with psychological response
A number of factors associated with psychological response have been found in other settings and warrant exploration in lung cancer, such as age, education, clinical stage, and tumor site. The association of any of these factors with psycholog- ical response in cancer patients was explored in our study.
Age
All of the 228 cancer patients were divided into >55 years old group and ≤55 years old group. The psychological responses were analyzed between the two groups, and there were no significant differences (Table 3). The gender groups were well balanced for age distribution and were ana- lyzed separately; the results (not shown) did not reach statis- tical significance, all p values were larger than 0.05.
Education
Educational background was analyzed to reflect its influence on psychology in cancer patients. All patients were divided into three groups: <high school graduate, high school gradu- ate, and college graduate. AVOVA results were as follows: p value and F value were 0.000 and 32.743 for negative emo- tion, 0.552 and 0.595 for positive attitude, and 0.001 and 7.763 for cognitive avoidance, respectively. There were lower scores of negative emotion and cognitive avoidance in
<high school graduate patients comparing to high school grad- uate patients and college graduate patients, as listed in Table 4.
Maybe this is due to“they that know nothing fear nothing”. Clinical stage
The males and females had equal proportions of stage II and stage IIIa patients. They were divided into stage II group and stage IIIa group, and the psychological responses were compared between the two groups. No significant differ- ences were found, as listed in Table 5. The males and Table 1 Demographic Characteristics.
Male Female
Total number (%) 120 (52.6%) 108 (47.4%) Age, mean (SD), year 57.19 (11.815) 55.31 (9.629) Cancer stage:
II 53 (44.2%) 55 (50.9%)
IIIa 67 (55.8%) 53 (49.1%)
Cancer site:
Lung 36 (30.0%) 37 (34.3%)
Gastrointestinal tract 47 (39.2%) 39 (36.1%) Head and neck 30 (25.0%) 14 (13.0%) Genitourinary tract 7 (5.8%) 18 (16.6%) Education
High school graduate 29 (24.2%) 36 (33.3%) High school graduate 66 (55.0%) 51 (47.2%) College graduate 25 (20.8%) 21 (19.5%) Family history
Negative* 23 (19.2%) 25 (23.1%)
Positive** 97 (80.8%) 83 (76.9%)
Note: No statistically significant differences at baseline between groups relative to mean age, cancer stage, education, and family history.
* No family member has cancer.
** One or more family members have cancer.
Table 2 Mini-MAC results of the comparison between males and females.
Male (n = 120) Female (n = 108)
t value p value NE1(SD) 18.57 (5.729) 20.91 (6.174) -2.969 0.003 PA2(SD) 16.66 (4.378) 14.83 (3.866) 3.321 0.001 CA3(SD) 7.61 (2.280) 7.54 (2.048) 0.247 0.805
1Negative Emotion.
2Positive Attitude.
3Cognitive Avoidance.
females were analyzed separately. We did not find any dif- ferences neither in males nor in females (data not shown).
The clinical stage did not associate with the psychological responses of cancer patients.
Tumor site
We investigated whether lung cancer patients have more negative emotion than non-lung cancer patients. For this pur-
pose, we compared the psychological responses between the two groups. We found that the lung cancer patients got higher scores of negative emotion and lower scores of posi- tive attitude than the non-lung cancer patients, and the results were statistically significant (Table 6). The same trend was found in female cancer patients in our study (Table 6). In male cancer patients, only a significantly higher score of negative emotion was found for lung cancer patients than that for non-lung cancer patients (Table 6).
Symptom burden
The physical symptom distress scale from the RSCL was used to reflect the symptom burden. It was expected that the symptom burden of females would be heavier than that of male group, and this was confirmed. The mean score of physical symptom distress scale of female group was 20.73 (SD = 7.438), and that of male group was 18.53 (SD = 7.508). The p value was 0.028 (t = -2.218).
Besides, we compared the psychological responses between small-cell lung cancer (SCLC) patients and non- small-cell lung cancer (NSCLC) patients. The SCLC Table 3 Comparison of≥55 years old group and <55 years old group.
>55 years old (SD), n = 131 ≤55 years old (SD), n = 97 t value p value
NE1(SD) 19.31 (6.488) 20.10 (5.351) –0.987 0.324
PA2(SD) 16.07 (4.464) 15.42 (3.894) 1.140 0.256
CA3(SD) 7.66 (2.022) 7.46 (2.359) 0.662 0.509
1Negative Emotion.
2Positive Attitude.
3Cognitive Avoidance.
Table 4 Results of Post hoc test of the comparison between the <high school graduate group, high school graduate group, and college graduate group.
<High4 (n = 65)
High5 (n = 117)
p value <High4 (n = 65)
College6 (n = 46)
p value High4 (n = 117)
College6 (n = 46)
p value
NE1 (SD)
15.26 (5.764) 21.91 (5.054) 0.000 15.26 (5.764) 20.13 (5.394) 0.000 21.91 (5.054) 20.13 (5.394) 0.056 PA2
(SD)
15.80 (4.040) 15.56 (4.340) 0.720 15.80 (4.040) 16.37 (4.265) 0.487 15.56 (4.340) 16.37 (4.265) 0.276 CA3
(SD)
6.72 (2.427) 7.83 (2.151) 0.001 6.72 (2.427) 8.13 (1.376) 0.001 7.83 (2.151) 8.13 (1.376) 0.412
1Negative emotion.
2Positive attitude.
3Cognitive avoidance.
4<High school graduate group.
5High school graduate group.
6College graduate group.
Table 5 Psychological results of stage II group and stage IIIa group.
Stage II (n = 108)
Stage IIIa (n
= 120)
t value p value NE1(SD) 20.01 (5.310) 19.38 (6.646) 0.790 0.430 PA2(SD) 15.80 (3.820) 15.79 (4.591) 0.008 0.993 CA3(SD) 7.56 (2.180) 7.59 (2.167) -0.125 0.900
1Negative emotion.
2Positive attitude.
3Cognitive avoidance.
patients (score 25.13) got higher scores of negative emotion than NSCLC patients (score 23.18), but this did not reach statistical significance (p = 0.052). The positive attitude (p = 0.769) and cognitive avoidance (p = 0.806) were no different between the two groups.
Discussion
Despite the fact that psychological response has a major impact in determining patients’quality of life, it is not rou- tinely assessed in cancer patients and the majority of pub- lished results of the clinical trials in cancer fail to address patients’ psychology on outcome. We found a significant higher level of negative emotion when they knew the news of cancer diagnosis and heavier symptom burden during the treatments in female cancer patients than males, which indi- cates that the psychological responses to the news of diagno- sis of cancer patients need to be systematically addressed in their overall management.
It was reported that the less negative emotion of illness had a more positive effect on psychological recovery of patients suffering from chronic diseases [3,5,7,28]. Studies have given good general evidence that the psychology of cancer patients between men and women was different [1,17,27]. Our data were consistent with them. Some studies reported increased negative emotion in the subsets of female patients [1,17,27]. Our data (Table 2) suggested that female cancer patients have more negative emotion and avoidance to the news of diagnosis and heavier symptom burden dur- ing the treatments, because the scores of negative emotion and symptom burden of female group were both higher when compared with male group. Gender might be the important factor which affected the psychological responses
of cancer patients. Whole cancer patients would experience the emotional reaction, such as fears of recurrence, worry, self-concept, and family and marital relationships. But the emotional reaction of females to cancer diagnosis might be stronger than males, and females might be more anxious about their features and their children. Moreover, women may conceal their feelings and emotional distress in an attempt to maintain a sense of normality and to avoid changes in routine patterns in life [2,6,18]. The attitude of an unfortunate life event to an external and stable causal factor can partly make the misery more bearable [14]. We found that the female and male cancer patients expressed various degree of positive attitude, but there was no statisti- cal significance.
We analyzed age, education, clinical stage, tumor site, and cell type (only in lung cancer patients) respectively in our study, because they may be associated with cancer patients’psychology. The result revealed that females show- ing more negative emotion and avoidance to the news of diagnosis were not influenced by age and clinical stage.
The One-Way AVOVA results showed that the negative emotion and cognitive avoidance were related with the edu- cational background, there were significant lower scores of negative emotion and cognitive avoidance in patients who did not go to high school. The lower the education level, the less knowledge they get about the poor prognosis of can- cer, and less worries and fears they experience.
Zhang and Shu [31] said that lung cancer patients had more depressive emotion than non-lung cancer patients, and our results were consistent with theirs. We found that lung cancer patients had more negative emotion than non- lung cancer patients whether in the whole patients or in the gender subgroups. This may partly due to the increasing prevalence of lung cancer and public health campaigns Table 6 Psychological results of lung cancer group and non-lung cancer group.
Whole patients Male Female
LC4 (n = 73)
NLC5 (n = 155)
t value p value LC4 (n = 36)
NLC5 (n = 84)
t value p value LC4 (n = 37)
NLC5 (n = 71)
t value p value
NE1 (SD)
24.22 (4.470)
17.54 (5.489)
9.078 0.000 22.17 (3.265)
17.02 (5.876)
4.928 0.000 26.22 (4.614)
18.14 (4.966)
8.213 0.000 PA2
(SD)
14.60 (4.1348)
16.35 (4.074)
-2.965 0.003 16.28 (4.633)
16.82 (4.283)
-0.622 0.535 12.97 (3.379)
15.80 (3.767)
-3.835 0.000 CA3
(SD) 7.79 (1.907)
7.47 (2.280)
1.051 0.294 7.58 (1.795)
7.62 (2.469)
-0.078 0.938 8.00 (2.014)
7.30 (2.038)
1.711 0.090
1Negative emotion.
2Positive attitude.
3Cognitive avoidance.
4Lung cancer.
5Non-lung cancer.
about lung cancer in recent years. The increasing prevalence and poor prognosis of lung cancer is publicized through var- ious ways, such as TV, newspaper, and Internet. The public- ity strengthened the negative emotional responses of lung cancer patients to the news of diagnosis. People got more knowledge about the prognosis of lung cancer than that of other cancers, so once they got this disease, they experienced more worries and fears.
Studies had demonstrated that negative emotion was more prevalent in patients with SCLC than those with NSCLC during their treatments [16,23]. Here we investi- gated whether the psychological responses of the SCLC patients differ from that of NSCLC patients when they knew the cancer diagnosis; the results indicated that there was no difference between them.
Throughout the cancer trajectory, including diagnosis, treatment, remission, and end of life, patients face numerous dynamic needs and difficult decisions [9,10,13]. The cancer diagnosis brings about an abrupt transition into a new world orbiting around cancer. By becoming more informed about the disease from physicians and nurses during their treat- ments and getting more support from family and friends, patients may have increased confidence, ask providers fewer, manage their disease more effectively, and have better coping and psychological adjustment [10]. The interventions to patient are critical to generating positive health outcomes.
Since females presented more negative emotion and avoid- ance when coping with cancer and more symptom burden during the treatments, clinicians and nurses should pay more attention to them. Social support from family and friends could partially decrease negative symptom and this directly related to improved quality of life [20]. Providing more information about the disease through clinicians and nurse and more support from family and friends, tackling the negative emotion actively, we may see great improve- ment of the quality of their life.
Some limitations of our study need to be noted. First, the sample size is not very large. But we compared the female cancer patients and male cancer patients, and the age, educa- tion, clinical stage, tumor site, and even cell type associated subgroups analysis were done; the results confirmed our hypothesis. An independent study with a larger sample may be more persuasive. The second one is the non- response bias. Although we tried our best to persuade all eligible patients to take part in, there were still few patients (18/260) refused. But this had little effect on the results.
In conclusion, our study suggested that female cancer patients, especially those who did not go to high school and those with lung cancer, have more negative emotion and symptom burden, comparing to male cancer patients.
Appropriate psychological intervention for female cancer patients deserves more attention.
Conflict of interest statement:the authors don’t have any conflict of interest to declare.
References
1. Angelopoulos NV, Tzivaridou D, Nikolaou N, Pavlidis AN (1995) Mental symptoms, hostility features and stressful life events in people with cancer. Acta Psychiatr Scand 92(1):44–50 2. Beatty L, Oxlad M, Koczwara B, Wade TD (2008) The psycho-
social concerns and needs of women recently diagnosed with breast cancer: a qualitative study of patient, nurse and volunteer perspectives. Health Expectations 11:331–42
3. Brady SS, Helgeson VS (1999) Social support and adjustment to recurrence of breast cancer. J Psychol Oncol 17(2):37-55 4. Breitbart W, Rosenfeld B, Pessin H, et al (2000) Depression,
hopelessness, and desire for hastened death in terminally ill patients with cancer. JAMA 284:2907–11
5. Cohen M (2002) Coping and emotion distress in primary and recurrent breast cancer paitents. Journal of Clinical Psychology in Medical Settings 9:245-51
6. Cowley L, Heyman B, Stanton M, Milner SJ (2000) How women receiving adjuvant chemotherapy for breast cancer cope with their treatment: a risk management perspective. J Adv Nurs 31:314–21
7. Dalal A (2000) Living with a chronic disease: healing and psy- chological adjustment in Indian society. Psychology and Devel- oping Societies 12:67–81
8. de Haes JC, van Knippenberg FC, Neijt JP (1990) Measuring psychological and physical distress in cancer patients: structure and application of the Rotterdam Symptom Checklist. Br J Can- cer 62(6):1034–8
9. DuBenske LL, Gustafson DH, Shaw BR, Cleary JF (2010) Web- based cancer communication and decision making systems: con- necting patients, caregivers, and clinicians for improved health outcomes. Med Decis Making 30(6):732–44
10. DuBenske LL, Wen KY, Gustafson DH, et al (2008) Caregivers’
needs at key experiences of the advanced cancer disease trajec- tory. Palliat Support Care 6:1–8
11. Ferlay J, Shin HR, Bray F, et al (2010) Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127 (12):2893–917
12. Ford S, Fallowfield L, Lewis S (1994) Can oncologists detect distress in their out-patients and how satisfied are they with their performance during bad news consultations? Br J Cancer 70:767–70
13. Hileman JW, Lackey NR (1990) Self-identified needs of patients with cancer at home and their home caregivers: a descriptive study. Oncol Nurs Forum 17(6):907–13
14. Ho SM, Fung WK, Chan CL, et al (2003) Psychometric proper- ties of the Chinese version of the Mini-Mental Adjustment to Cancer (Mini-MAC) scale. Psychooncology 12:547–56 15. Hoogerwerf MA, Ninaber MK, Willems LN, Kaptein AA (2012)
“Feelings are facts”: illness perceptions in patients with lung can- cer. Respir Med 106(8):1170–6
16. Hopwood P, Stephens RJ (2000) Depression in patients with lung cancer: prevalence and risk factors derived from quality-of-life data. J Clin Oncol 18(4):893–903
17. Jacobs-Lawson JM, Schumacher MM, Hughes T, Arnold S (2010) Gender differences in psychosocial responses to lung can- cer. Gender Med 7(2):137–48
18. Knobf M (2011) Clinical update: psychosocoal responses in breast cancer survivors. Semin Oncol Nurs 27(3):e1–e14
19. Lynch J, Goodhart F, Suanders Y, O’Connor SJ (2011) Screening for psychological distress in patients with lung cancer: results of a clinical audit evaluating the use of the patient Distress Ther- mometer. Support Care Cancer 19:193–202
20. Manning-Walsh J (2004) Social support as a mediator between symptom distress and quality of life in women with breast cancer.
J Obstet Gynecol Neonatal Nurs 34:482–93
21. McClain CS, Rosenfeld B, Breitbart W (2003) Effect of spiritual well-being on end-of-life despair in terminally-ill cancer patients.
Lancet 361:1603–7
22. Messina G, Lissoni P, Marchiori P, et al (2010) Enhancement of the efficacy of cancer chemotherapy by the pineal hormone mel- atonin and its relation with the psychospiritual status of cancer patients. J Res Med Sci 15(4):225–8
23. Montazeri A, Milroy R, Hole D, et al (1998) Anxiety and depres- sion in patients with lung cancer before and after diagnosis:
findings from a population in Glasgow, Scotland. J Epidemiol Community Health 52(3):203–4
24. Passik SD, Dugan W, McDonald MV, et al (1998) Oncologists’ recognition of depression in their patients with cancer. J Clin Oncol 16:1594–600
25. Sharp L, Carsin AE, Timmons A (2012) Associations between cancer-related financial stress and strain and psychological well- being among individuals living with cancer. Psychooncology 22 (4):745–55
26. Slovacek L, Slovackova B, Slanska I, et al (2009) Cancer and depression: a prospective study. Neoplasma 56(3):187–93 27. Sneed NV, Edlund B, Dias JK (1992) Adjustment of gynecologi-
cal and breast cancer patients to the cancer diagnosis: compari- sons with males and females have other cancer sites. Health Care for Women International 13(1):11-22
28. Stanton AL, Snider PR (1993) Coping with a breast cancer diag- nosis: a prospective study. Health Psychol 12(1):16–23 29. Valente SM, Saunders JM, Cohen MZ (1994) Evaluating depres-
sion among patients with cancer. Cancer Pract 2:65–71 30. Watson M, Homewood J, Haviland J, Bliss JM (2005) Influence
of psychological response on breast cancer survival: 10-year follow-up of a population-based cohort. Eur J Cancer 41 (12):1710–4
31. Zhang JD, Shu ZR (2006) The incidence if depression and its affecting factors in patients with malignant tumors. Acta Acade- miae Medicinae Qingdao Universitatis 42(4):2
