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 atteintesde 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

Abstract Background: Patients’ well-being may be affectedby the cancer diagnosis. Psychological response is part of areaction to the news of cancer diagnosis. Little publisheddata concerns the gender difference of psychologicalresponses to the news of cancer diagnosis and its influenceon the symptom burden. The aim of the study is to verify thehypothesis that female cancer patients have more negativeemotion 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 Chineseversion of Mini-Mental Adjustment to Cancer scale, andsymptom burden was measured by the physical symptomdistress scale from the Rotterdam Symptom Checklist. SPSS13.0 was used.Results: Female cancer patients got higher scores of negativeemotion (P = 0.003), cognitive avoidance (P = 0.001), andsymptom burden (P = 0.028) than males. Patients withdegrees lower than high school got lower scores of negativeemotion and cognitive avoidance. Lung cancer patients gothigher scores of negative emotion and lower scores of posi-tive attitude.Conclusion: Female cancer patients, especially those whodid not go to high school and those with lung cancer, havemore negative emotion and symptom burden, comparing tomales. Appropriate psychological intervention for femalecancer patients deserves more attention.

Keywords Cancer · Female · Psychological response ·Negative emotion · Symptom burden

Résumé Contexte : Le diagnostic du cancer peut avoir unimpact 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 différenceentre les sexes en matière de réactions psychologiques àl’annonce d’un diagnostic de cancer et son influence surla charge psychique liée aux symptômes. L’objectif del’étude est de vérifier l’hypothèse selon laquelle les femmesatteintes d’un cancer ressentent davantage d’émotionsnégatives et la charge psychique liée aux symptômes, parrapport aux hommes.Sujets et méthodes : Deux cent vingt-huit patients atteints decancer 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 mentaleau cancer) et la charge psychique liée a été déterminé parl’échelle de détresse liée aux symptômes issus de la liste decontrôle des symptômes de Rotterdam. Le logiciel SPSS13.0 a été utilisé.Résultats : Les patientes atteintes de cancer ont obtenu desscores plus élevés d’émotions négatives (p = 0,003),d’évitement cognitif (p = 0,001) et de charge psychiqueliée aux symptômes (p = 0,028) que les hommes. Lespatients 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 atteintsd’un cancer du poumon ont obtenu des scores plus élevésd’émotions négatives et de plus faibles scores d’attitudepositive.Conclusion : Les femmes atteintes de cancer, en particulierles femmes n’ayant pas suivi d’études secondaires et lesfemmes atteintes d’un cancer du poumon, ressentent davan-tage d’émotions négatives et la charge psychique liée auxsymptômes par rapport aux hommes. Une intervention psy-chologique appropriée pour les femmes atteintes de cancermérite une plus grande attention.

Mots clés Cancer · Femme · Réaction psychologique ·Émotions négatives · Fardeau des symptômes

Z.-M. Niu (*) · Y.-S. WangDepartment of Thoracic Oncology, Cancer Center,State Key Laboratory of Biotherapy, West China Hospital,Sichuan University, Chengdu 610041, PR Chinae-mail : niuzm06@126.com

Y. Li · X.-Y. Peng · X.-Y. Cui · Y.-K. Wu · C.-S. LiangWest China Hospital, Sichuan University, Chengdu 610041,PR China

Psycho-Oncol. (2013) 7:175-181DOI 10.1007/s11839-013-0431-5

Introduction

The global burden of cancer has increased largely in recentyears. About 12.7 million cancer cases are estimated to haveoccurred in 2008 world-wide, with 56% of the cases in theeconomically developing world [11]. Important aspects ofa patient’s well-being may be adversely affected by thediagnosis of cancer [4,16,21]. Yet in the field of cancer,reports of clinical trials are often limited to the impact oftoxicity, treatment on survival, or physical symptoms, ratherthan inclusive of psychological responses such as negativeemotion [16].

Psychological response may obviously be part of a reac-tion to the news of cancer diagnosis; in many patients it willpersist, affecting the general management and symptom con-trol [16]. It is well documented that patients themselves donot disclose their emotion unless asked, and doctors wereprimarily influenced by patients’ outward signs, whichmay be misleading, and seriously underestimated negativeemotion, although the importance of psychological function-ing had been emphasized [12,24,29]. A direct consequenceof 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 receivetreatment, there is little published data concerning the genderdifference of psychological responses to the news of cancerdiagnosis and its influence on the symptom burden. In ourstudy, we made the hypothesis that female cancer patientshave more negative emotion and symptom burden, compar-ing to males.

The aim of the study is to verify the hypothesis. We usedthe 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 themand age, educational background, clinical stage, and tumorsite; and recorded the symptom burden for each. Our resultsconfirmed the hypothesis.

Methods

Participants

The clinical records and psychological and symptomaticdata 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 beforethe inclusion date; clinical stage II~IIIa; awareness of theircancer diagnosis; no apparent serious intellectual and func-tional impairment; be in a similar economic state, not badnor good; and receiving primary chemotherapy treatment.This study was approved by the Ethical Committee of Sich-uan University, and written informed consent was obtainedfrom all participants.

All patients meeting the eligibility criteria were identifiedfrom hospital records, and most of them approached duringthe normal hospital in-patient visits, when they were asked ifthey would be willing to take part in this study assessing thepsychological 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 patientsagreed to participate in the psychological assessment, andthey were divided into two groups: male group and femalegroup.

Procedure

Patients were assessed by self-administered questionnaireand they completed the study measures at 1–3 months afterdiagnosis.

The Chinese version of the Mini-MAC scale was used tomeasure the psychological response to the news of diagnosisin our study. It is a 29-item self-report measurement tooldesigned for use in patient settings to assess psychologicalresponse to cancer, and it concludes Negative Emotion,Positive Attitude, and Cognitive Avoidance.

The physical symptom distress scale from the RotterdamSymptom 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 theirprimary chemotherapy treatments.

Patients’ symptom experience of both psychological andphysical ranged from “not at all” to “very much.” Scoresgiven 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 ofpsychological response or symptom burden.

Statistical methods

T-Test was used to compare the age, psychological response,clinical stage, tumor site, and symptom burden betweengroups. Crosstabs were used to test the family history. Forthe possible predictor variable education, One-Way AVOVAwas used. The statistical software we used was SPSS13.0.We indicated a significant result with p < 0.05.

176 Psycho-Oncol. (2013) 7:175-181

Result

The detailed information of all participants is documented inTable 1. There were no statistically significant differencesat baseline between males and females relative to meanage, education, clinical stage, tumor site, and family history(all the p value were > 0.05).

Psychological response to cancer

We compared the psychological responses to cancer betweenmales and females; the scores for them are listed in Table 2.A significantly higher score of negative emotion was foundfor female patients than that for male patients, for whom thep value was less than 0.05 (Table 2). And the scores of posi-tive attitude of females were significantly lower than that ofmales. All cancer patients expressed various degree ofavoidance, but there was no statistical significance betweengroups.

Gender might just play an important role in the psycho-logical responses of cancer patients. In order to demonstratethis, the influence of some probable factors must be takeninto consideration.

Probable factors associated with psychologicalresponse

A number of factors associated with psychological responsehave been found in other settings and warrant exploration inlung cancer, such as age, education, clinical stage, and tumorsite. 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 yearsold group and ≤55 years old group. The psychologicalresponses were analyzed between the two groups, andthere were no significant differences (Table 3). The gendergroups 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 influenceon psychology in cancer patients. All patients were dividedinto three groups: <high school graduate, high school gradu-ate, and college graduate. AVOVA results were as follows: pvalue and F value were 0.000 and 32.743 for negative emo-tion, 0.552 and 0.595 for positive attitude, and 0.001 and7.763 for cognitive avoidance, respectively. There werelower 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 andstage IIIa patients. They were divided into stage II groupand stage IIIa group, and the psychological responses werecompared 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

1 Negative Emotion.2 Positive Attitude.3 Cognitive Avoidance.

Psycho-Oncol. (2013) 7:175-181 177

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 psychologicalresponses of cancer patients.

Tumor site

We investigated whether lung cancer patients have morenegative emotion than non-lung cancer patients. For this pur-

pose, we compared the psychological responses between thetwo groups. We found that the lung cancer patients gothigher scores of negative emotion and lower scores of posi-tive attitude than the non-lung cancer patients, and theresults were statistically significant (Table 6). The sametrend was found in female cancer patients in our study(Table 6). In male cancer patients, only a significantly higherscore of negative emotion was found for lung cancer patientsthan that for non-lung cancer patients (Table 6).

Symptom burden

The physical symptom distress scale from the RSCL wasused to reflect the symptom burden. It was expected thatthe symptom burden of females would be heavier than thatof male group, and this was confirmed. The mean scoreof physical symptom distress scale of female group was20.73 (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 responsesbetween 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

1 Negative Emotion.2 Positive Attitude.3 Cognitive 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

1 Negative emotion.2 Positive attitude.3 Cognitive avoidance.4 <High school graduate group.5 High school graduate group.6 College 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

1 Negative emotion.2 Positive attitude.3 Cognitive avoidance.

178 Psycho-Oncol. (2013) 7:175-181

patients (score 25.13) got higher scores of negative emotionthan NSCLC patients (score 23.18), but this did not reachstatistical significance (p = 0.052). The positive attitude(p = 0.769) and cognitive avoidance (p = 0.806) were nodifferent between the two groups.

Discussion

Despite the fact that psychological response has a majorimpact 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 addresspatients’ psychology on outcome. We found a significanthigher level of negative emotion when they knew the newsof cancer diagnosis and heavier symptom burden during thetreatments 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 intheir overall management.

It was reported that the less negative emotion of illnesshad a more positive effect on psychological recovery ofpatients suffering from chronic diseases [3,5,7,28]. Studieshave given good general evidence that the psychology ofcancer patients between men and women was different[1,17,27]. Our data were consistent with them. Some studiesreported increased negative emotion in the subsets of femalepatients [1,17,27]. Our data (Table 2) suggested that femalecancer patients have more negative emotion and avoidanceto the news of diagnosis and heavier symptom burden dur-ing the treatments, because the scores of negative emotionand symptom burden of female group were both higherwhen compared with male group. Gender might be theimportant factor which affected the psychological responses

of cancer patients. Whole cancer patients would experiencethe emotional reaction, such as fears of recurrence, worry,self-concept, and family and marital relationships. But theemotional reaction of females to cancer diagnosis might bestronger than males, and females might be more anxiousabout their features and their children. Moreover, womenmay conceal their feelings and emotional distress in anattempt to maintain a sense of normality and to avoidchanges in routine patterns in life [2,6,18]. The attitude ofan unfortunate life event to an external and stable causalfactor can partly make the misery more bearable [14]. Wefound that the female and male cancer patients expressedvarious 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 inour study, because they may be associated with cancerpatients’ psychology. The result revealed that females show-ing more negative emotion and avoidance to the news ofdiagnosis were not influenced by age and clinical stage.

The One-Way AVOVA results showed that the negativeemotion and cognitive avoidance were related with the edu-cational background, there were significant lower scores ofnegative emotion and cognitive avoidance in patients whodid 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 hadmore depressive emotion than non-lung cancer patients,and our results were consistent with theirs. We found thatlung cancer patients had more negative emotion than non-lung cancer patients whether in the whole patients or in thegender subgroups. This may partly due to the increasingprevalence 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

1 Negative emotion.2 Positive attitude.3 Cognitive avoidance.4 Lung cancer.5 Non-lung cancer.

Psycho-Oncol. (2013) 7:175-181 179

about lung cancer in recent years. The increasing prevalenceand 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 lungcancer patients to the news of diagnosis. People got moreknowledge about the prognosis of lung cancer than that ofother cancers, so once they got this disease, they experiencedmore worries and fears.

Studies had demonstrated that negative emotion wasmore prevalent in patients with SCLC than those withNSCLC during their treatments [16,23]. Here we investi-gated whether the psychological responses of the SCLCpatients differ from that of NSCLC patients when theyknew the cancer diagnosis; the results indicated that therewas no difference between them.

Throughout the cancer trajectory, including diagnosis,treatment, remission, and end of life, patients face numerousdynamic needs and difficult decisions [9,10,13]. The cancerdiagnosis brings about an abrupt transition into a new worldorbiting around cancer. By becoming more informed aboutthe disease from physicians and nurses during their treat-ments and getting more support from family and friends,patients may have increased confidence, ask providersfewer, manage their disease more effectively, and have bettercoping and psychological adjustment [10]. The interventionsto patient are critical to generating positive health outcomes.Since females presented more negative emotion and avoid-ance when coping with cancer and more symptom burdenduring the treatments, clinicians and nurses should paymore attention to them. Social support from family andfriends could partially decrease negative symptom and thisdirectly related to improved quality of life [20]. Providingmore information about the disease through clinicians andnurse and more support from family and friends, tacklingthe 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, thesample size is not very large. But we compared the femalecancer patients and male cancer patients, and the age, educa-tion, clinical stage, tumor site, and even cell type associatedsubgroups analysis were done; the results confirmed ourhypothesis. An independent study with a larger samplemay be more persuasive. The second one is the non-response bias. Although we tried our best to persuade alleligible 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 cancerpatients, especially those who did not go to high schooland those with lung cancer, have more negative emotionand symptom burden, comparing to male cancer patients.Appropriate psychological intervention for female cancerpatients deserves more attention.

Conflict of interest statement: the authors don’t have anyconflict of interest to declare.

References

1. Angelopoulos NV, Tzivaridou D, Nikolaou N, Pavlidis AN(1995) Mental symptoms, hostility features and stressful lifeevents 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 withbreast cancer: a qualitative study of patient, nurse and volunteerperspectives. Health Expectations 11:331–42

3. Brady SS, Helgeson VS (1999) Social support and adjustment torecurrence 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 illpatients with cancer. JAMA 284:2907–11

5. Cohen M (2002) Coping and emotion distress in primary andrecurrent breast cancer paitents. Journal of Clinical Psychologyin Medical Settings 9:245-51

6. Cowley L, Heyman B, Stanton M, Milner SJ (2000) How womenreceiving adjuvant chemotherapy for breast cancer cope withtheir treatment: a risk management perspective. J Adv Nurs31:314–21

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) Measuringpsychological and physical distress in cancer patients: structureand 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 healthoutcomes. 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 worldwideburden of cancer in 2008: GLOBOCAN 2008. Int J Cancer 127(12):2893–917

12. Ford S, Fallowfield L, Lewis S (1994) Can oncologists detectdistress in their out-patients and how satisfied are they withtheir performance during bad news consultations? Br J Cancer70:767–70

13. Hileman JW, Lackey NR (1990) Self-identified needs of patientswith cancer at home and their home caregivers: a descriptivestudy. 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 toCancer (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 lungcancer: prevalence and risk factors derived from quality-of-lifedata. 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 inbreast cancer survivors. Semin Oncol Nurs 27(3):e1–e14

180 Psycho-Oncol. (2013) 7:175-181

19. Lynch J, Goodhart F, Suanders Y, O’Connor SJ (2011) Screeningfor psychological distress in patients with lung cancer: results ofa 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 betweensymptom 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 spiritualwell-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 ofthe efficacy of cancer chemotherapy by the pineal hormone mel-atonin and its relation with the psychospiritual status of cancerpatients. 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 EpidemiolCommunity 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 ClinOncol 16:1594–600

25. Sharp L, Carsin AE, Timmons A (2012) Associations betweencancer-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 anddepression: 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. HealthCare 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) Influenceof psychological response on breast cancer survival: 10-yearfollow-up of a population-based cohort. Eur J Cancer 41(12):1710–4

31. Zhang JD, Shu ZR (2006) The incidence if depression and itsaffecting factors in patients with malignant tumors. Acta Acade-miae Medicinae Qingdao Universitatis 42(4):2

Psycho-Oncol. (2013) 7:175-181 181