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Controlled Study of Fatigue, Quality of Life, and Somatic and Mental Morbidity in Epithelial Ovarian Cancer Survivors: How Lucky Are the Lucky Ones?

Astrid H. Liavaag, Anne Dørum, Sophie D. Fosså, Claes Tropé, Alv A. Dahl

From the Department of Gynecology, Sorlandet Hospital, Arendal; and the Department of Gynecological Oncology and The Cancer Clinic, Department of Clinical Cancer Research, Rikshospitalet-Radiumhospitalet, University of Oslo, Oslo, Norway

Address reprint requests to Astrid H. Liavaag, MD, Department of Gynecology, Sorlandet Hospital HF, Serviceboks 605, 4809 Arendal, Norway; e-mail: astrid.liavaag{at}sshf.no

	ABSTRACT

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

 
Purpose: There are few studies of somatic and mental morbidity in epithelial ovarian cancer survivors (EOCSs). The aim of this controlled, cross-sectional study was to explore fatigue, quality of life (QOL), and somatic and mental morbidity in EOCSs.

Patients and Methods: Among 287 EOCSs treated according to protocols at The Norwegian Radium Hospital between 1977 and 2003, 189 patients (66%) participated. Information was collected by a questionnaire containing demographic and morbidity items and self-rating scales. Internal comparisons of various subgroups of EOCSs were performed, and EOCSs were compared with age-adjusted controls from the general population.

Results: Minimal differences were observed relating to somatic and mental morbidity, fatigue, and QOL between EOCSs with and without relapse, long or short follow-up time, and prognostic index status. Chronic fatigue was found in 22% (95% CI, 16% to 28%), and only body image was significantly associated with chronic fatigue in multivariable analyses. EOCSs showed significantly more somatic and mental morbidity, somatic complaints, use of medications, and use of health care services than controls. The levels of anxiety and fatigue were also significantly higher in EOCSs than in controls, whereas the levels of depression and of several QOL dimensions were lower. The prevalence of chronic fatigue was 12% among controls.

Conclusion: EOCSs had more somatic and mental morbidity, more fatigue, poorer QOL, and used more medication and health services than controls. Minimal differences were observed between various EOCS subgroups. Health care professionals should try to improve and be attentive to the health of EOCSs.

	INTRODUCTION

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Few studies have investigated the somatic and mental health, fatigue, and health-related quality of life (QOL) in survivors of epithelial ovarian cancer (EOCSs) who have survived more than 1 year after primary treatment. Given that the number of EOCSs disease free for more than 2 years has been low, Stewart et al¹ characterized such survivors as "the lucky ones"; however, such EOCSs are gradually becoming more numerous. Multimodal treatment is the main reason for this positive development, but only a minority of EOCSs become permanently tumor free; the majority experience relapses with multiple courses of chemotherapy during the years.² In her review, Lockwood-Rayermann² emphasized the need for more data regarding the situation of EOCSs, and particularly in relation to long-term observations.

Stewart et al¹ reported that among 200 EOCSs without evidence of active disease for 2 years, 98% regarded their health as good or excellent, whereas 54% had current pain or discomfort. EOCSs reported better mental health and equivalent fatigue levels compared with controls. Among 98 EOCSs without evidence of active disease for more than 6 months, Holzner et al³ found that 33% had fatigue. Wenzel et al⁴ reported that in 49 EOCSs without evidence of active disease, 75% had little or no problems with physical well-being, 6% had depression, 14% had fear of recurrence, and 20% had long-term adverse effects.

On the basis of a considerable sample size of EOCSs and access to normative data (NORM), the aims of this cross-sectional, follow-up study of somatic and mental morbidity, fatigue, and QOL in EOCSs were to compare subgroups of EOCSs in relation to relapse, currently on/off treatment, follow-up time, and prognostic index; to explore factors in EOCSs associated with caseness of chronic fatigue; and to compare findings in EOCSs with age-adjusted controls from the general population.

	PATIENTS AND METHODS

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Sample Selection
We included EOCSs from the Department of Gynecological Oncology, Rikshospitalet-Radiumhospitalet Medical Center (until 2004, The Norwegian Radium Hospital) with more than 18 months survival. The women included were 20 to 70 years old at the time of the survey and were treated according to protocol for International Federation of Gynecology and Obstetrics (FIGO) stage I to III epithelial ovarian cancer. We had to go back to July 15, 1977, to acquire a sample size sufficient to fill the statistical requirements. The selection criteria were fulfilled by 297 EOCSs who were alive by September 2004, and these patients were invited by mail to take part in the study. One reminder was sent to the nonrespondents after 4 weeks.

After additional examination of their medicals records, we excluded 10 EOCSs: two respondents and two nonrespondents who received pelvic radiotherapy as primary treatment in the end of the 1970s, three nonrespondents who received pelvic radiotherapy because of concurrent endometrial cancer, one respondent and one nonrespondent who had stromal ovarian cancer, and one nonrespondent who received bleomycin, etoposide, and cisplatin treatment because of unusual histology.

Treatment Principles
All patients had primary surgery at local hospitals or at our department with or without subsequent chemotherapy according to established protocols.⁵ Two main treatment modalities were used during the recruitment period: radical surgery only, or surgery and postoperative chemotherapy dependent on FIGO stage, histology, and ploidy.

Platinum-based chemotherapy represented the most frequent systemic treatment. Paclitaxel was incorporated into the combination chemotherapy in the 1990s.⁶ The majority of patients in our sample received combined carboplatin and paclitaxel as first-line treatment, but nine received single-agent therapy with cisplatin. Relapses were treated with various types of chemotherapy. Combination- or single-drug second-line therapy was administered (including paclitaxel, carboplatin, and tamoxifen) depending on the time since primary treatment (before or after 6 months) and site of relapse. Four EOCSs received radiotherapy after relapse in lymph nodes, brain, or bone.

Measurements
Education was categorized into three levels based on the number of school years completed. Paired relation consisted of those married or cohabiting. Having paid work was defined as income from employment or independent business. All comorbid diseases were self-reported, and diagnoses were not confirmed by the general practitioners of EOCSs. Musculoskeletal diseases were defined as a physician's diagnosis of osteoporosis, fibromyalgia, arthrosis, or other long-standing musculoskeletal diseases. Somatic complaints included "considerable distress" last year caused by nausea, heartburn, diarrhea, constipation, tachycardia, dyspnea, or bloating. Hormone replacement therapy was reported as current use of gonadal hormones, whereas other medication was reported as regular use last year. Daily smoking related to current consumption of cigarettes. Level of physical activity was defined according to Thorsen et al.⁷

The Fatigue Questionnaire (FQ) assesses the presence and intensity of fatigue symptoms.⁸ Seven items assess physical fatigue, and four items assess mental fatigue, and they were added together to provide the total fatigue score. Patients with chronic fatigue (CF) were identified according to the given procedure.⁸ In our sample of EOCSs, the internal consistency of the fatigue symptoms items were = .91 and = .87 in the NORM 2004.

The Hospital Anxiety and Depression Scale (HADS) consists of a depression and an anxiety subscale.⁹ Cases of HADS-defined anxiety disorder (HADS-A) or depression (HADS-D) were defined by a score of 8 on these subscales.⁹ The internal consistency for HADS-A was = .88 and for HADS-D was = .84 in our EOCSs sample, and was = .81 and = .79 for Nord-Tröndelag Health Study (HUNT) controls, respectively.

The European Organisation and Treatment of Cancer Quality of Life Questionnaire-C30 (QLQ-C30) consists of 30 items comprising five functional scales, an overall QOL/global health scale, three symptom scales, and six single-symptom items.¹⁰ The scores are transformed onto a 0 to 100 scale: on the functional scales, higher score represents better functioning, whereas on the symptom scales, higher score means more symptoms. In the EOCSs sample, the internal consistencies of the following functions were physical, = .76 (NORM 2005, = .77); role, = .87 (NORM 2005, = .90); emotional, = .88 (NORM 2005, = .85); cognitive, = .71 (NORM 2005, =. 66); social, = .88 (NORM 2005, = .86); and overall QOL/global health, = .89 (NORM 2005, = .91).

Body image scale (BIS) is a 10-item self-rating scale developed to show changes in body image in cancer patients.¹¹ The questionnaire evaluates how the patient feels about her appearance and about changes due to disease. Each item is scored on a four-point Likert scale and higher BIS score represents poorer body image. The internal consistency in the EOCSs sample was = .92.

Prognostic index in EOCSs was constructed for this study by scoring the presence of established prognostic factors: age at diagnosis, FIGO stage, relapse within 6 months, primary treatment modality, and follow-up time.^5,6 On the basis of the index sum score, EOCSs were allocated to a worst, medium, or best prognostic group. Details are shown in the footnote to Table 1.

NORM Samples
To obtain NORM samples, the Cancer Clinic performed two similar studies 1 year apart. Using public address lists, an anonymous age-representative sample of the Norwegian female population (3,500 females in 2004 and 2005) age 20 to 79 years received a questionnaire containing the QLQ-C30 in 2004 and the FQ in 2005, as well as questions about demography and use of medication. Among the women invited in 2004, 41% responded, and 988 were 30 to 71 years old, free of cancer, and had completed QLQ-C30. In the 2005 survey, 38% responded; of them, 957 delivered completed FQ. For the QLQ-C30, we drew one control for each EOCS based on 5-year age-groups (NORM 2004) and used the same procedure for the FQ (NORM 2005).

Statistical Analysis
Data were analyzed with SPSS-PC version 12.0 (SPSS Inc, Chicago, IL). Continuous data were analyzed by t tests and univariate analysis of variance with adjustment for confounders. Categoric data were analyzed with Pearson's ² or Fisher's exact test. Nonparametric tests were applied when appropriate for skewed distributions. Significant findings on continuous measures were calculated as Cohen's effect sizes and values more than .50 were considered as clinically relevant.¹⁴ The association with patients with CF (dependent variable) and relevant independent variables were explored by logistic regression analyses. The associations were expressed as odds ratios with 95% CIs. Because multiple comparisons were performed, the level of significance was set at P < .01 and all tests were two tailed.

Ethics
The study was approved by the Regional Ethics Review Board of South-Norway and the Norwegian Data Inspectorate. All EOCSs provided written informed consent.

	RESULTS

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Disease Groups and Attrition Analysis
Among the 287 EOCSs eligible for the study, 189 (66%) participated. We separated the 189 EOCS respondents into 130 (69%) patients who never had a relapse (nonrelapse group) and 59 (31%) who had a relapse (relapse group). All of the EOCSs in the relapse group had their relapse within 6 months after primary treatment. In the relapse group, 17 EOCS had received chemotherapy during the last 6 months (on-treatment group) and 42 had not received chemotherapy during the last 6 months (off-treatment group).

A comparison of EOCSs respondents (n = 189) and nonrespondents (n = 98) showed that except for longer time since primary treatment among the respondents (mean 6.3 v 4.4 years, P = .003), no significant differences in relapse rate or other clinical variables were observed.

EOCS With and Without Relapse
Significantly higher proportions of EOCS in FIGO stage III and with chemotherapy were found in the relapse compared with the nonrelapse group (Table 2).

Other EOCS Subgroups
On the basis of a cutoff of 5 years, 76 (40%) EOCSs were long-term survivors and 113 (60%) were short-term survivors. According to the Prognostic Index, 54 (29%) EOCSs belonged to the best group, 99 (52%) belonged to the medium group, and 36 (19%) belonged to the worst group (Table 1). Fifty-seven (30%) EOCSs had surgery only as primary treatment, whereas 132 (70%) have received postoperative chemotherapy (Table 1). No significant differences were observed regarding somatic diseases, somatic complaints, anxiety or depression, fatigue, or for QLQ-C30 scales of functioning and global QOL/health status, regarding survival length, prognostic index, or primary treatment subgroups (data not shown).

Associations With Caseness of CF
Demographic and cancer-related variables did not show any significant associations with caseness of CF in univariate analyses (data not shown). The QLQ-C30 emotional, physical, and cognitive functions, and the symptoms of nausea, pain, dyspnea, sleeplessness, reduced appetite, as well as anxiety, use of antidepressants/sedatives, and body image were significantly associated with caseness of CF in univariable analyses (Table 3). In multivariate analyses, only poor body image was significantly associated with such caseness.

Comparisons of EOCSs and HUNT
Given that only global QOL/health status showed a significant difference between EOCSs with and without relapse, we treated all EOCSs as one group in the comparisons with the HUNT controls. The level of education was significantly higher in EOCSs compared with HUNT controls, whereas a significantly lower proportion of the latter group held a paid job. The prevalence of fibromyalgia and any musculoskeletal disease as well as regular physical activity was significantly higher in EOCSs compared with HUNT controls (Appendix Table A1, online only). Complaints about nausea, diarrhea, and constipation in the last year were significantly more common in EOCSs (Table 4). The use of hormone replacement therapy, other types of medication, and the use of health services also were significantly more common in EOCSs. The level of anxiety and the prevalence of HADS-defined anxiety were significantly higher in EOCSs, whereas the level of depression was lower than in HUNT controls.

	DISCUSSION

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Comparisons of EOCSs with and without relapse did not show any significant differences regarding somatic or mental morbidity, fatigue, or QOL, except for QLQ-C30 overall QOL/global health that was poorer in the relapse group. CF was observed in 22.2% (95% CI, 16.3% to 28.1%) of all EOCSs, which was higher than in controls (12.2%; 95% CI, 7.5% to 16.9%), but not significantly so. Only body image was significantly associated with CF in multivariable analyses. EOCSs subgroup analyses of prognostic index, survival time, and primary treatment did not show any differences on fatigue, QOL, or mental or somatic morbidity. Compared with age-adjusted controls, EOCSs had significantly more musculoskeletal diseases and more distressing GI symptoms. Use of medication was also significantly more frequent in EOCSs, as was visits to their regular general practitioners. Compared with controls, the QLQ-C30 cognitive, emotional, and social functions were significantly lower in EOCSs. Significantly higher levels of anxiety but lower levels of depression were observed compared with controls.

Our finding of a considerable proportion of CF patients in the EOCS group is in accordance with the findings of Holzner et al³ and in contrast to those of Stewart et al.¹ The reduction of QOL functions was in contrast to the findings of Wenzel et al.⁴ The findings of positive somatic and mental health reported by Wenzel et al⁴ and Stewart et al¹ were not confirmed in our comparisons with age-adjusted controls. EOCSs have considerably more somatic and mental morbidity, use of medication, and consumption of health services compared with age-adjusted controls. However, these three studies had shorter follow-up time than our study.

We also compared EOCSs with relapse on and off treatment for the last 6 months, which showed that those on treatment had poorer social function than those off treatment. However, small numbers make type II statistical errors a definite limitation of these comparisons.

To our knowledge, this is the first study to compare EOCSs with and without relapse, and we also note that all relapses occurred within 6 months after primary treatment, which is less favorable prognostically. The surprising lack of intergroup difference could be explained by adaptation and response shift in the years after primary treatment. We presume that after having survived the first 18 months, mental distress may have been reduced and QOL improved due to acceptance of patients’ new life situation. The higher frequency of physically active individuals can indicate that EOCSs are more conscious about their health and lifestyle than were the controls.

The level of anxiety is increased and several QLQ-C30 functions decreased compared with the age-adjusted NORM samples. However, the level of depression was significantly lower in EOCSs, which was not related to the higher proportion of EOCSs using sedatives or antidepressants. In general, anxiety is a reaction to danger in the future, whereas depression is a reaction to loss.¹⁵ We therefore presume that EOCSs still worry about relapse and the course of their disease, whereas the initial loss of being diagnosed with cancer has been processed mentally over time, and in that perspective EOCSs have a lower level of depression than controls.

The 66% respondent rate is considered to be quite good, particularly given that many EOCSs were treated several years ago and some of the questionnaires contained questions about sensitive familial and sexual issues. We have used international instruments and questionnaires that are well validated and with good psychometric properties. We also present data on the nonrespondents that showed few significant differences, and allow us to draw conclusions about EOCSs more generally. The age-matching of the controls emphasizes the validity of our findings.

One limitation may be the 29-year inclusion period. During this time span, several types of first-line chemotherapy were also used; however, not in our sample of survivors. Given that the majority received chemotherapy with platinum and paclitaxel, we found subanalyses on that factor less relevant. Primary treatment with surgery and postoperative chemotherapy was considered to be similar during this time period.

The relapse group contained 59 EOCSs, and with a significance level of P < .01, our study has low statistical power, and only quite large effect sizes will be identified with confidence.

A major limitation of the study is the fairly low participation rate of the NORM samples, which is a common problem in surveys of the general population without reminders or incentives. We do not know to what degree the scores of the participants are representative for the nonparticipants. Other Norwegian studies have demonstrated only modest differences in prevalence estimates and sociodemographic distribution when comparing results by individuals responding after a reminder and initial responders.^16-18

In conclusion, EOCSs have significantly more somatic diseases and complaints, higher scores on fatigue and anxiety, and poorer QOL compared with NORM samples. The groups with and without relapse, as well as other subgroups, were quite similar regarding somatic and mental morbidities, fatigue, and QOL. The subgroup of patients with relapses on treatment during the last 6 months scored worse in these domains compared with those treated for relapse a longer time ago. EOCSs may be considered lucky because they have survived for considerable time, but they pay a price of increased morbidity and fatigue and poorer QOL on a long-term basis. General practitioners, gynecologists, and oncologists should pay attention to the health care of EOCSs, and not simply remind them that they are lucky to be alive.

	AUTHORS’ DISCLOSURES OF POTENTIAL CONFLICTS OF INTEREST

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

 
The authors indicated no potential conflicts of interest.

	AUTHOR CONTRIBUTIONS

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

 
Conception and design: Astrid H. Liavaag, Anne Dørum, Alv A. Dahl

Financial support: Anne Dørum

Administrative support: Anne Dørum, Sophie D. Fosså, Claes Tropé

Provision of study materials or patients: Astrid H. Liavaag, Anne Dørum, Claes Tropé

Collection and assembly of data: Astrid H. Liavaag, Anne Dørum

Data analysis and interpretation: Astrid H. Liavaag, Anne Dørum, Sophie D. Fosså, Alv A. Dahl

Manuscript writing: Astrid H. Liavaag, Anne Dørum, Sophie D. Fosså, Claes Tropé, Alv A. Dahl

Final approval of manuscript: Astrid H. Liavaag, Anne Dørum, Sophie D. Fosså, Claes Tropé, Alv A. Dahl

	Appendix

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	NOTES

 
Supported by The Norwegian Foundation for Health and Rehabilitation (Grant No. 55002/001) through the Norwegian Cancer Society (A.H.L.). The Nord-Trøndelag Health Study (the HUNT study) is a collaboration between HUNT Research Centre, Faculty of Medicine, Norwegian University of Science and Technology (Verdal), Norwegian Institute of Public Health, and Nord-Trøndelag County Council.

Presented in part at the annual meeting of the Norwegian Gynecological Association, September 1, 2006, Oslo, Norway.

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

	REFERENCES

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

 
1. Stewart DE, Wong F, Duff S, et al: What doesn't kill you makes you stronger: An ovarian cancer survivor survey. Gynecol Oncol 83: 537-542, 2001[CrossRef][Medline]

2. Lockwood-Rayermann S: Survivorship issues in ovarian cancer: A review. Oncol Nurs Forum 33: 553-562, 2006[CrossRef][Medline]

3. Holzner B, Kemmler G, Meraner V, et al: Fatigue in ovarian carcinoma patients: A neglected issue. Cancer 97: 1564-1572, 2003[CrossRef][Medline]

4. Wenzel LB, Donnelly JP, Fowler JM, et al: Resilience, reflection, and residual stress in ovarian cancer survivorship: A gynecologic oncology group study. Psychooncology 11: 142-153, 2002[CrossRef][Medline]

5. Berek JS, Hacker NF: Practical Gynecologic Oncology (ed 4). Philadelphia, PA, Lippincott, Williams and Wilkins, 2005, pp 443-494

6. Friedlander ML: Prognostic factors in ovarian cancer. Semin Oncol 25: 305-314, 1998[Medline]

7. Thorsen L, Nystad W, Stigum H, et al: The association between self-reported physical activity and prevalence of depression and anxiety in long-term survivors of testicular cancer and in general population sample. Support Care Cancer 13: 637-646, 2005[CrossRef][Medline]

8. Chalder T, Berelowitz G, Pawlikowska T, et al: Development of a fatigue scale. J Psychosom Res 37: 147-153, 1993[CrossRef][Medline]

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10. Aaronson NK, Ahmedzai S, Bergman B, et al: The European Organization for Research and Treatment of Cancer QLQ-C30: A quality of life instrument for use in international trials in oncology. J Natl Cancer Inst 85: 365-376, 1993[Abstract/Free Full Text]

11. Hopwood P, Fletcher I, Lee A, et al: A body image scale for use with cancer patients. Eur J Cancer 37: 189-197, 2001[Medline]

12. Holmen J, Midthjell K, Krüger Ö, et al: The Nord-Tröndelag Health Study 1995-97 (HUNT 2): Objectives, contents, methods and participation. Nor Epidemiol 13: 19-32, 2003

13. Norwegian University of Science and Technology: HUNT. http://www.hunt.ntnu.no/

14. Cohen J: Statistical Power Analysis for the Behavioral Sciences (ed 2). Hillsdale, NJ, Lawrence Erlbaum Associates, 1988

15. Hales RE, Yudosky SC, Talbott JA The American Psychiatric Press Textbook of Psychiatry (ed 3). Washington, DC, American Psychiatric Press, 1999

16. Sogaard AJ, Selmer R, Bjertness E, et al: The Oslo Health Study: The impact of self-selection in a large, population-based survey. Int J Equity Health 3: 3, 2004[CrossRef][Medline]

17. Selmer R, Sogaard AJ, Bjertness E, et al: The Oslo Health study: Reminding the non-responders—effects on prevalence estimates. Nor Epidemiol 13: 89-94, 2003

18. Stigum H, Magnus P, Veierod M, et al: Impact on sexually transmitted disease spread of increased condom use by young females, 1987-1992. Int J Epidemiol 24: 813-820, 1995[Abstract/Free Full Text]

Submitted September 15, 2006; accepted February 15, 2007.

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