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Survival After a Psychoeducational Intervention for Patients With Cutaneous Malignant Melanoma: A Replication Study

Ellen H. Boesen, Sidsel H. Boesen, Kirsten Frederiksen, Lone Ross, Karin Dahlstrøm, Grethe Schmidt, Jesper Næsted, Christen Krag, Christoffer Johansen

From the Institute of Cancer Epidemiology, Danish Cancer Society; Department of Plastic Surgery, Herlev Hospital, University of Copenhagen, Herlev Ringvej, Copenhagen County; Department of Plastic Surgery and Burn Unit, Rigshospitalet, University of Copenhagen, Copenhagen; and the Department of Plastic and Recunstructive Surgery, Roskilde University Hospital, Roskilde, Denmark

Address reprint requests to Ellen H. Boesen, MD, Institute of Cancer Epidemiology, Danish Cancer Society, Strandboulevarden 49, DK-2100 Copenhagen, Denmark; e-mail: ellen{at}cancer.dk

	ABSTRACT

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Purpose: The results of a randomized, intervention study done in 1993 of psychoeducation for patients with early-stage malignant melanoma showed a beneficial effect on recurrence and survival 6 years after the intervention. In the present study, we replicated the study with 258 Danish patients with malignant melanoma. We also compared recurrence and survival among the participants in the randomized study with 137 patients who refused to participate.

Patients and Methods: We randomly assigned 262 patients with primary malignant melanoma to a control or an intervention group. Patients in the intervention group were offered six weekly 2-hour sessions of psychoeducation. Participants and nonparticipants were followed up for vital status and recurrence 4 to 6 years after surgical treatment. Prognostic factors (thickness of the tumor and lymph node status), sex, and age were adjusted for in a Cox regression model (proportional hazards regression) to derive an adjusted survival rate ratio and an adjusted relapse-free survival rate ratio, with 95% CIs.

Results: The hazard ratio was 1.30 (95% CI, 0.5 to 3.5) for survival and 0.73 (95% CI, 0.3 to 1.9) for recurrence. Being a nonparticipant increased the risk for death by more than two-fold (hazard ratio, 2.26; 95% CI, 1.0 to 5.2) over that of participants.

Conclusion: Psychoeducation did not increase survival or the recurrence-free interval among patients with malignant melanoma; however, nonparticipants had a statistically significantly greater risk for death than participants.

	INTRODUCTION

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In 1993, Fawzy et al reported the results from a randomized trial of a psychoeducational intervention among patients with malignant melanoma and found a survival benefit for patients in the intervention arm, with a similar trend for time to recurrence.¹ Psychoeducation is a structured, time-limited intervention that consists of health education, enhancement of problem-solving skills, stress management (eg, relaxation techniques), and psychological support.^2,3 Recently, Fawzy et al reported the results of a 10-year follow-up for survival and recurrence in the same patients⁴ and found that participation in the intervention still predicted better survival after adjustment for the effects of other known prognostic indicators (Breslow depth and sex), but the trend for later recurrence had disappeared.⁴

Other studies of the effect of psychosocial intervention on cancer survival indicate that psychosocial intervention affects the prognosis only for patients with early-stage cancer, as the natural course of more advanced stages might obviate a possible effect of psychosocial factors. Four psychosocial intervention studies—one of 120 persons with various advanced-stage cancers and three of patients with metastatic breast cancer (n = 66, 121, and 235 patients)—did not find an effect of the intervention on survival.^5-8 Three further studies, however, showed an effect on the survival of 86 patients with advanced-stage breast cancer,⁹ 271 patients with various cancer types known to have a poor prognosis,¹⁰ and 375 patients who were heterogeneous in terms of stage, but not of cancer type.¹¹ Besides the studies by Fawzy et al,^1,4 another US study of 303 women with early-stage breast cancer receiving adjuvant chemotherapy failed to show a difference in survival between those who received 20 sessions of weekly group therapy plus three relaxation classes, and those who had three relaxation classes alone,¹² thus precluding any clear conclusion concerning the effect of different intervention strategies.

The intervention used by Fawzy can be characterized as a brief psychoeducational intervention, which differs from the long-term existential group therapy used by Spiegel et al.⁹ In the study reported by McCorkle et al,¹¹ a clinical assessment was added to the psychosocial intervention; the positive effect of this approach might indicate an effect on prognosis of an optimized medical treatment. Two studies were conducted with a view to repeating the positive effects reported by Spiegel et al, but no positive effects were found.^6,8

We previously reported positive effects of a psychoeducational intervention on psychological distress and coping ability in a randomized study of Danish patients with malignant melanoma,¹³ which was a replication of the study by Fawzy et al. In our study, analysis 6 months later showed that the intervention enhanced effective coping and reduced psychological distress in comparison with standard surgical treatment, but the effect was small and short-term.¹³ We now report the effect of the intervention on disease recurrence and mortality up to 5 years after primary surgery. We also report the results for patients who refused to participate in the randomized study. To the best of our knowledge, no study has included survival data on nonparticipants, even though the participation rates in the randomized psychosocial intervention studies published so far range from 40% to 80%, leaving room for the possibility that selection of patients into the studies might reduce the generalizability of the results.^14,15

	PATIENTS AND METHODS

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Selection Criteria
Eligible patients had to be 18 to 70 years of age with cutaneous malignant melanoma of T1 to 4, N1a–2a, M₀¹⁶ diagnosed and treated in eastern Denmark. Patients were contacted by a project nurse in outpatient clinics 3 to 12 weeks after surgery, and those who gave oral and written consent completed a baseline questionnaire and were then randomized to the intervention or the control group. Random assignment was performed with a computer program, which generated a balanced number of random assignments to the two groups in blocks of randomly varying sizes of six, eight, or 10 patients. This ensured equal distribution of patients in the two groups and reduced possible confounding by season or calendar time. Figure 1 shows the design of the study, with the numbers of patients at each stage. Between February 1, 1999, and June 15, 2001, 420 eligible patients were identified, of whom 21 (5%) were excluded before randomization on the basis of information obtained at the recruitment interview. Of the 399 patients who met the inclusion criteria, 262 (66%) agreed to participate, and 137 (34%) refused because of the distance involved, lack of time, or feeling no need for support. Of the 131 patients originally assigned to the intervention group, three were excluded from the survival analyses: one had received a diagnosis of cancer before inclusion, one received immunotherapy, and one died before the start of the intervention. Another 16 patients (12%) dropped out of the intervention group before it started (nine patients) or after one session (seven patients), but were followed up for recurrence and survival and were included in the survival analyses. Two more patients dropped out shortly after randomization, one due to disappointment because of control status and the other for an unknown reason. The first patient refused to be followed up and was excluded from the survival analyses, leaving 130 patients in the control group.

View larger version (22K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 1. Trial profile outlining randomized controlled trial design with numbers of patients in each group. (*) All drop-out patients were followed up for recurrence and survival and included in the survival analyses. () One control patient did not want any follow-up and was excluded from the survival analyses. () One patient had a testes cancer diagnosis before inclusion, one received immunotherapy and one patient died before start of the intervention.

Follow-Up
According to the medical guidelines of the Danish Melanoma Group,¹⁷ patients with malignant melanoma are followed up for 5 years at an outpatient clinic if no recurrence or second primary tumor has occurred, and the patient does not have dysplastic nevi syndrome. The patients are followed up every 3 months for 2 years and then twice a year for the following 3 years. The plastic surgeon registers the status of the patient, with regard to malignant melanoma and the date of the clinical examination, on a continuation sheet designed by the Danish Melanoma Group. When there is a recurrence, the continuation sheet is completed by a plastic surgeon, with the date of the recurrence, verified by a pathological report. A research assistant (an MD with a license in plastic surgery) blinded to the randomization status of the patients in the study reviewed the patients' medical records between March 1 and June 30, 2005, and checked all continuation sheets for the date of recurrence. The vital status of all patients was obtained by using their unique personal identification numbers, assigned by the Central Population Register to all Danish residents who were alive on April 1, 1968, or born thereafter. The Register holds information on vital status and is updated daily. Data on recurrence and survival were available for all patients.

Questionnaire
Patients in both groups were asked to complete the baseline questionnaire on sociodemographics 6 and 12 months after surgery. The Profile of Mood States scale was used to measure psychological distress,¹⁸ and coping styles were elicited from a questionnaire originally developed to measure the ability of patients to cope with newly diagnosed AIDS, but revised for cancer patients.¹³ The revised questionnaire comprises 50 items to assess cognitive and behavioral means of dealing with serious illness. The results of the analysis of responses to the questionnaire are reported elsewhere.¹³

Group Intervention
Before conducting the Danish study, the principal investigator (E.H. Boesen) visited Nancy Fawzy, RN, DNS, at the John Wayne Cancer Institute (Los Angeles, CA) who conducted the original intervention in collaboration with I. Fawzy.¹ E.H. Boesen followed Nancy Fawzy's program and had access to the intervention manual² and to additional material. The Danish intervention was organized into six sessions lasting approximately 2 hours each, conducted over a 6-week period for groups of a maximum of 10 patients. The intervention was as described in the manual developed by Fawzy et al² and comprised education in health behavior with regard to malignant melanoma, stress management, problem-solving, and mutual support, as described in detail elsewhere.¹³

A few changes were made for the Danish study. The health education component was conducted by specialized health staff from the plastic surgery department and not the group leader; however, the group leader was present at every session to provide psychological support. Coping methods were discussed on the basis of the patients' experiences, and problems on the basis of questions about the topics outlined in the intervention manual.² In the original study, these topics were discussed on the basis of illustrations of coping scenarios. No other changes were made. As in the original study, the control group did not receive any intervention. Both groups were followed up routinely at outpatient clinics.

Statistical Analysis
Data for patients in the intervention group were analyzed independently of the number of educational sessions they attended (intention-to-treat principle). Lack of attendance was due to illness, work obligations, time or distance involved, or no need for support. Baseline data were compared using ² tests for categorial variables and the Mann-Whitney U test for the continuous variable age and tumor thickness. No differences were found between the randomization groups. Nonparticipants had significantly lower socioeconomic status than participants (data not shown). ²⁸

Mortality was compared by Kaplan-Meier survival curves to account for unequal follow-up times.¹⁹ Crude testing of whether the survival curves were identical was performed with a log-rank statistic. We estimated the association between patient group (intervention, control, and nonparticipants) and the end points recurrence and all-cause mortality in the Cox proportional hazard model. Time since operation was used as the time axis, and adjustment for well-known prognostic factors gave an adjusted survival rate ratio and an adjusted relapse-free rate ratio, with 95% CIs. Associations between baseline total mood disturbance, coping method, and outcome (recurrence and survival) were estimated for all participants with adjustment for the covariates Breslow depth, sentinel node status, sex, and age. Patients were followed up for recurrence and survival from the day of the primary operation. The software used was the SAS statistical package (SAS Institute, Cary, NC) v.9.0 for the Unix platform.

	RESULTS

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Eight of the 128 patients in the intervention group died during follow-up, and recurrent disease was found in 11 patients. In the control group, eight of 130 patients died during the same period, and recurrence of malignant melanoma was diagnosed in seven patients. In the group of nonparticipants, 19 of 137 died and 12 of 137 had recurrent disease (Table 1). The cumulative disease-free and survival rates of the groups indicate that nonparticipants survived for a shorter time than the intervention and control groups, for which there was no difference in survival (Fig 2). No difference in time to recurrence was observed among the three patient groups. Breslow depth and lymph node status were significant prognostic factors for time to recurrence and length of survival (Table 2).

View larger version (16K): [in this window] [in a new window] [PowerPoint Slide for Teaching]   Fig 2. Kaplan-Meier recurrence and survival curves for patients assigned to the intervention and the control group and nonparticipants.

The baseline scores of the intervention and control groups for profile of mood and dealing with illness are presented in Table 3. None of the scores predicted time to recurrence or death. Analysis of the scores 6 months after the intervention showed no change (data not shown).

	DISCUSSION

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The different outcomes of these two almost-identical studies may have several explanations. The difference in survival might be due to the large difference in the survival time of controls in the two studies, which were 29% and 6%, respectively, indicating that the patients in the control group of the original study might have differed significantly from the intervention group with regard to unknown prognostic factors. For instance, diagnosis of affected sentinel nodes was not available when the study was conducted. Furthermore, our study had more statistical power, as we had more than double the number of patients.

We found only short-term beneficial effects of the intervention on mood and effective coping,¹³ suggesting that it is unlikely that a psychoeducational intervention would enhance survival. This conclusion is supported by the analysis results of the prognostic value of baseline scores for mood and coping, none of which predicted time to recurrence or survival. Furthermore, our patients had low levels of baseline distress, leaving little room for improvement with an intervention such as that offered. To identify a survival benefit among patients with low rates of distress, a substantially larger sample size would be needed. A real effect of an intervention on recurrence and survival could be demonsrated only if the study cohort were screened before random assignment and if patients in most need were offered the intervention.

It is not yet known which psychological and social factors predict survival. In studies of 426 and 125 patients with malignant melanoma, avoidance, positive mood, no concern about the disease or about the impact of the disease on the family,²¹ and anger²² predicted a poorer outcome. Canada et al found that personality type could not be used to determine risk for either recurrence or death from malignant melanoma. ²³ In studies of 303 and 235 patients with breast cancer participating in psychosocial group interventions, the intervention improved various psychosocial factors, but did not prolong the time to recurrence or survival.^8,12 In another study, health-related quality of life had no prognostic value for 448 patients with nonmetastatic breast cancer.²⁴ The most convincing evidence that psychological factors influence survival was found for hopelessness or helplessness, depression,²⁵ and minimizing the impact of disease.^22,26,27

In our study, nonparticipation in the intervention increased morbidity by more than two-fold, after control for other risk factors. This surprising result might be explained by the socioconomic status of the nonparticipants, as the responses to the questionnaire showed that they had a lower socioeconomic status than participants.²⁸ Socioeconomic status has been shown to be correlated with survival,²⁹ and a recent study in England and Wales during 1986 to 1990, 1991 to 1995, and 1996 to 1999 showed that while survival from most cancers improved during the 1990s, the deprivation gap in survival between rich and poor was wider for cancers diagnosed in the late 1990s than in the late 1980s.³⁰ A study in England of patients with cancers of the upper GI tract showed a significant association between social deprivation and death after esophagectomy.³¹

Even in a relatively homogeneous society like that of Sweden, where mammography and standard treatment regimens are offered within the tax-funded health care system, one study showed that the risk for death after breast cancer was 37% higher among patients of low socioeconomic status than those of high status (hazard ratio for high versus low, 0.73; 95% CI, 0.54 to 0.99).³²

The 40% of nonparticipants who completed the baseline questionnaire had lower levels of distress than participants,²⁸ indicating that the level of baseline distress was not likely to be the explanation for the worse survival of the nonparticipants. The nonparticipants had significantly lower scores for adaptive coping, but the level of avoidance coping was no higher than that of participants; it is only the latter that appears to be linked to survival.²⁶ Poorer survival might also be due to nonadherence to health-promoting principles, which is probably correlated with socioeconomic status.

The result of this study adds to the results of a number of well-conducted studies on survival after participation in a psychosocial intervention, with both patients with metastatic disease^6-8 and patients with primary cancer.¹² The overall conclusion from the present and other studies is that psychosocial intervention does not prolong the time to recurrence and does not improve survival after diagnosis and treatment of cancer. Further studies are needed before definitive conclusions can be drawn about the predictive value of psychological factors and the effects of interventions on recurrence and survival. Nevertheless, there is strong evidence that the psychological distress of patients with cancer can be reduced by participation in interventions, justifying the use of psychosocial support for cancer survivors in clinical practice.

	Authors' Disclosures of Potential Conflicts of Interest

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... Author Contributions REFERENCES

 
The author(s) indicated no potential conflicts of interest.

	Author Contributions

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION Authors' Disclosures of... Author Contributions REFERENCES

 
Conception and design: Ellen H. Boesen, Christoffer Johansen

Provision of study materials or patients: Karin Dahlstrøm, Grethe Schmidt, Jesper Næsted, Christen Krag

Collection and assembly of data: Ellen H. Boesen

Data analysis and interpretation: Ellen H. Boesen, Sidsel H. Boesen, Kirsten Frederiksen

Manuscript writing: Ellen H. Boesen, Sidsel H. Boesen, Kirsten Frederiksen, Lone Ross, Karin Dahlstrøm, Grethe Schmidt, Jesper Næsted, Christen Krag, Christoffer Johansen

Final approval of manuscript: Christoffer Johansen

	ACKNOWLEDGMENTS

 
We thank the plastic surgery departments of Rigshospitalet, Herlev, and Roskilde Hospital for excellent cooperation; Nancy Fawzy, RN, DNSc, the John Wayne Cancer Institute, for kindly letting the author (E.H.B.) watch a group intervention; and all the patients who participated in the study.

	NOTES

 
Supported by the Psychosocial Research Committee, The Danish Cancer Society (Grants No. 9722559 and PP01016) and the IMK Foundation (Grant No. 5322569).

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

	REFERENCES

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21. Brown JE, Butow PN, Culjak G, et al: Psychosocial predictors of outcome: Time to relapse and survival in patients with early stage melanoma. Br J Cancer 83:1448-1453, 2000[CrossRef][Medline]

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Submitted January 21, 2007; accepted September 25, 2007.

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This Article Abstract Full Text (PDF) Purchase Article View Shopping Cart Alert me when this article is cited Alert me if a correction is posted Services Email this article to a colleague Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Save to my personal folders Download to citation manager Rights & Permissions Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Boesen, E. H. Articles by Johansen, C. Search for Related Content PubMed PubMed Citation Articles by Boesen, E. H. Articles by Johansen, C. Related Articles Related Editorial