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Anticipated Versus Actual Emotional Reactions to Disclosure of Results of Genetic Tests for Cancer Susceptibility: Findings From p53 and BRCA1 Testing Programs

From the Divisions of Population Sciences and Pediatric Oncology, Dana-Farber Cancer Institute, Departments of Psychiatry and Medicine, Harvard Medical School, and Children’s Hospital, Boston, MA, and Departments of Medicine and Genetics, University of Pennsylvania, Philadelphia, PA.

Address reprint requests to Andrea F. Patenaude, PhD, Dana-Farber Cancer Institute, 44 Binney St, Boston MA 02115; email andrea_patenaude{at}dfci.harvard.edu

	ABSTRACT

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PURPOSE: We examined the ability of individuals undergoing genetic testing for cancer susceptibility in two structured research protocols to accurately anticipate emotional reactions to disclosure of their test result. We explored whether accuracy of emotional anticipation was associated with postdisclosure psychologic adjustment.

METHODS: Data from 65 individuals were analyzed; 24 members of Li-Fraumeni cancer syndrome families were tested for p53 mutations (all 24 were unaffected), and 41 subjects with hereditary breast-ovarian cancer susceptibility were tested for BRCA1 mutations (34 were unaffected and seven were affected). Subjects were from families in which a germline mutation had been previously identified. At the pretest session, subjects rated the extent to which they anticipated feeling each of six emotional states (relief, happiness, sadness, guilt, anger, and worry) after disclosure that they did or did not carry the familial mutation. After receiving their test result, they rated their feelings on the same scale of emotions for the appropriate condition. Extent of accuracy and association with psychologic distress at 6 months, as assessed with standardized measures, were evaluated.

RESULTS: Overall, mean levels of emotional reactions after receiving test results were not different from those anticipated before result disclosure. However, affected BRCA1 carriers experienced higher levels of anger and worry than they had anticipated. Underestimation of subsequent distress emotions related to test result was associated with a significant increase in general psychologic distress at 6 months.

CONCLUSION: Unaffected individuals in cancer-predisposition testing programs are generally accurate in anticipating emotional reactions to test results. However, cancer patients may underestimate their distress after disclosure of positive results and could benefit from intervention strategies.

	INTRODUCTION

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ONE IMPORTANT goal of counseling before genetic tests for cancer predisposition is to enable individuals to make informed decisions about testing. A typical genetic counseling session includes extensive discussion of the benefits, limitations, and risks of testing.^1-3 Consideration of medical benefits, risks, and limitations can be guided by information based on expert opinion⁴ and scientific data when available. However, evaluation of psychologic risks and benefits relies primarily on personal values and previous experiences. Structured encouragement to consider the potential emotional impact of disclosure of a positive result and disclosure of a negative result is a commonly used strategy in genetic counseling.² The extent to which this approach helps individuals considering genetic testing to conceptualize the experience is not known. In other circumstances, rehearsal has reduced distress after stressful events.^5-7 Individuals who accurately anticipate how they will react emotionally to the forthcoming disclosure of their test result may be less likely to experience psychologic difficulties after genetic testing. In turn, they may be more likely to comply with surveillance and prevention recommendations.⁸

We investigated the relationship between anticipated and actual reactions to disclosure of results of genetic tests for cancer susceptibility, using data from two cancer-predisposition testing programs through the Dana-Farber Cancer Institute (DFCI)—one involving p53 testing of members of Li-Fraumeni cancer syndrome families and one involving BRCA1 testing of members of breast-ovarian cancer syndrome families. We also explored whether the accuracy of emotional anticipation was associated with postdisclosure psychologic adjustment. In both syndromes, an autosomal dominantly inherited mutation in a known cancer susceptibility gene is associated with a high risk of multiple early-onset cancers.^9-12

	METHODS

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Subjects
Beginning in 1994, germline p53 testing was offered to members of families from the Li-Fraumeni Cancer Family registry at DFCI, which includes families of which a germline p53 mutation has been identified in at least one member. The BRCA1 testing program was offered to members of high-risk breast and ovarian cancer families from DFCI and the University of Pennsylvania in which a BRCA1 mutation had been documented. In both programs, eligible subjects were men and women age 18 years or older. In the p53 genetic testing program, subjects had at least a 25% risk of carrying the familial mutation, based on their position in the pedigree; in the BRCA1 testing program, subjects had a risk of 12.5% or greater of being a mutation carrier. The p53 testing program was restricted to individuals who had never had cancer; the BRCA1 testing program included cancer patients. In both programs, participants were widely dispersed throughout the United States. All subjects provided informed consent in the context of genetic testing protocols approved by the participating institutional review boards.

Thirty-two individuals from nine extended kindreds were enrolled onto the p53 genetic testing program, attended a pretest education session, and provided blood samples for testing. Four participants opted not to receive their test result, and disclosure of test results to two patients was postponed by program staff because of significant baseline psychopathology. Of the 26 individuals who received test results in the program, two had missing data regarding anticipated reactions to test results. The following analyses are therefore based on 24 (92%) of the 26 individuals who received their test results in the p53 testing program.

Fifty-three individuals from 16 kindreds were enrolled onto the BRCA1 testing program and attended the pretest session. Among them, eight declined to receive test results. Of the 45 individuals who received test results in the program, four did not provide data on actual emotional reactions for this study. Thus, the following analyses are based on 41 (91%) of the 45 participants who received test results in the BRCA1 testing program.

Genetic Testing Programs
The p53 and the BRCA1 genetic testing programs have been described in detail.¹³ Both programs included extensive genetic counseling and psychologic assessment. Genetic counseling was provided to each participant in a pretest education session and a result disclosure session using structured interviews to ensure that participants received uniform information. Topics covered at the pretest session included standard items of informed consent for genetic testing¹⁴ and consideration of potential psychologic effects of both positive and negative results on the participant as well as the subsequent impact on other family members. Printed and audiovisual materials were also given to participants. Individual risk of carrying the familial mutation was provided. Blood samples were drawn from consenting participants at the conclusion of this session. The disclosure session included review of medical recommendations and discussion of the possible individual and family impact of the test results.

Measures
For research and safety purposes, the p53 and the BRCA1 testing programs included extensive psychologic assessment by means of semistructured interviews and standard measures.¹³ Anticipated reactions to genetic testing results were assessed during psychologic interviews conducted either concurrently with the pretest genetic counseling session (p53 testing program) or within 7 to 10 days of the session (BRCA1 testing program). During the psychologic interview, participants were asked first to imagine that they had received their test result and then to answer questions about their expected emotional reactions after disclosure. In a first scenario, participants were invited to imagine how they would feel if they learned that they did not have the familial mutation. Participants rated their expected emotional states of relief, happiness, sadness, guilt, anger, and worry on 5-point scales ranging from 1 ("not at all") to 5 ("very intensively"). After this, participants were asked to assume that they did carry the familial mutation and to apply the same scale to the same range of emotions.

After receiving their genetic test result, participants rated their actual emotional reactions using the same ratings of emotional states. This rating was performed during the psychologic interview immediately after the result disclosure session (p53 testing program) or within 7 to 10 days of the session (BRCA1 testing program).

In both programs, participants were asked to complete standardized measures of general emotional distress at program entry (baseline) and then 6 months after result disclosure. Subjects in the p53 testing program completed the Symptom Checklist-90—Revised (SCL-90-R).¹⁵ Those in the BRCA1 testing program completed the Brief Symptom Inventory (BSI).¹⁶ The SCL-90-R is a widely used 90-item self-report psychologic symptom inventory; the BSI is a 53-item brief form of the SCL-90-R. There is strong support of the equivalence of the SCL-90-R and the BSI.^15,16 The BSI defines psychologic distress in terms of the same nine symptom dimensions and three global indices as those of the SCL-90-R, and correlations between the two measures are high.^15,16 To ensure comparability between distress scores from the p53 and BRCA1 testing programs, we recalculated scores from the SCL-90-R based on the 53 items of the BSI. Among subjects in the p53 testing program, Pearson’s correlation coefficients between the 90-item and the 53-item versions were 0.99 and 0.97 at the pretest session and at 6 months, respectively. The following analyses are based on the Global Severity Index (GSI), a summary scale reflecting the extent of overall symptomatic distress, using GSI T-scores (mean ± SD, 50 ± 10) based on separate norms available for males and females in nonclinical populations. GSI scores have been used as a measure of psychologic adjustment in previous genetic testing studies.¹⁷

Analyses
Because of variations between data collection procedures in the two genetic testing programs, analyses were either carried out separately for the two groups of subjects or performed simultaneously for all subjects, controlling for the potential confounding effect of testing program. Univariate comparisons of predisclosure and postdisclosure reactions were conducted using paired t tests. All significance levels reported are two-sided. Multivariate analysis of factors potentially predicting postdisclosure psychologic adjustment was performed using a hierarchic multiple regression analysis of 6-month global GSI T-scores. In the first step of this analysis, the following variables were initially considered for inclusion in the model on the basis on their a priori importance for the genetic testing process: genetic testing program (BRCA1 v p53), cancer status (affected v unaffected), genetic testing result (positive for mutation v negative for mutation), and pretest psychologic distress scores. Because of collinearity between testing program and cancer status (only the BRCA1 testing program included individuals who had had cancer), two dummy variables that incorporate both testing program and cancer status were used: the first was created to compare affected and nonaffected individuals from the BRCA1 testing program, and the second was created to compare nonaffected BRCA1 testing program participants and p53 testing program participants. Sex and age were omitted because of their low univariate associations with 6-month distress (P .20). In the second step of the analysis, two dummy variables were created for accuracy of anticipation of (1) positive emotions (happiness, relief) and (2) negative emotions (sadness, guilt, anger, and worry). One dummy variable was made to compare individuals who overestimated at least one positive emotion and those who did not; the other dummy variable was made to compare participants who underestimated one or more negative emotions and those who did not.

	RESULTS

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Participant Characteristics
Participants enrolled onto the p53 testing program differed from those in the BRCA1 testing program in terms of sociodemographics and disease characteristics (Table 1). Specifically, p53 testing program participants were more often male, younger, and less educated compared with subjects enrolled onto the BRCA1 testing program. In addition, the BRCA1 testing program included seven participants (17%) who had previously had cancer, whereas the p53 testing program was limited to individuals without cancer.

View larger version (33K): [in this window] [in a new window]   Fig 1. Anticipated emotional reactions to hypothetical disclosure of negative and positive test results.

View larger version (15K): [in this window] [in a new window]   Fig 2. Proportions of carriers whose actual emotional reactions were rated lower (overestimation) or higher (underestimation) compared with their anticipated reactions

The results of hierarchic regression analysis of 6-month psychologic distress scores are listed in Table 3. The control variables entered in the first step of the analysis accounted for 34% of the variance in 6-month psychologic distress (P .001), with pretest distress and the dummy variable comparing nonaffected participants in the BRCA1 testing program and p53 testing program participants both making significant independent contributions. In the second step of the analysis, the accuracy of anticipation variables produced a statistically significant increment in R² (R² = 0.09, P .05), although only the dummy variable created for anticipation of distress emotions made a significant contribution (P .05). Specifically, as evidenced by the final beta weight, the underestimation at the pretest session of one or more distress emotions was associated with a seven-point increase in the psychologic distress (GSI) score 6 months after result disclosure, despite controlling for other variables in the model. The final model accounted for 44% of the variance in 6-month psychologic distress (GSI) scores (P = .001).

	DISCUSSION

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Learning how anticipated reactions relate to actual reactions may be useful in the provision of cancer genetic counseling. The observation that most affected BRCA1 carriers felt more distressed than they had anticipated after learning their carrier status suggests that there may be a role for postdisclosure psychologic counseling of individuals who have had cancer, to help in resolution of distress experienced after disclosure. However, this finding should be confirmed, given the small number of affected BRCA1 carriers in our study. It was assumed that cancer patients in cancer families would expect that they were mutation carriers and would believe that "the worst had already happened," and thus it was assumed that disclosure of a positive test result would elicit little emotion. Nonetheless, most BRCA1 carriers who had had cancer underestimated their distress reactions to disclosure. After disclosure, cancer patients may have a greater awareness of their own increased risk of second cancer and may be more conscious of the genetic contribution to an increased risk of cancer in their offspring. Receipt of a positive genetic test result may also reactivate distress relating to cancer diagnosis and treatment, so that the emotional distress reported may include response to the recent genetic test result and also response to prior cancer issues. Until information from larger cohorts is available to clarify these issues, it may be important to ensure that individuals with cancer contemplating genetic testing receive careful preparation and support. A cancer patient’s reaction to disclosure may have far-reaching implications, because cancer patients are often the first in their families to be tested for a gene mutation. Hence, if a deleterious mutation is found in a cancer patient, the response of the patient may influence decisions about testing among other at-risk family members for whom testing would be informative.

Our finding of a significant association between accuracy of anticipation of distress reactions to testing and 6-month psychologic distress scores raises questions about causal mechanisms involved in psychologic adaptation to results of genetic testing for cancer susceptibility. This observation plus the fact that relatively low levels of distress have been reported in other programs offering extensive genetic counseling^18-20 may suggest such counseling is useful in helping individuals to predict their reactions and is protective against psychologic distress. There is also some evidence that patients who anticipate difficulty in coping with genetic test results may be less likely to be tested for cancer susceptibility.²² This implies that individuals undergoing testing are more likely to be those who think they can cope with the forthcoming genetic information. Further research is also needed to clarify this issue.

Our data also shed some light on the experience of guilt among individuals undergoing genetic testing for cancer risk. Modest levels of guilt were reported in anticipation of positive results and in anticipation of negative results. Postdisclosure guilt ratings remained low, suggesting that on average, participants did not experience strong guilt after disclosure of either a positive or a negative test result. In most cases, guilt may be less of an issue for genetic testing program participants who actually receive results than has been reported in hypothetical circumstances.^23-26

Estimating the accuracy of anticipated emotions is a difficult task and may be subject to several biases. First, the simple act of asking about anticipated reactions could be viewed as an intervention that may have enhanced participants’ awareness of the potential emotional impact of their test result. It is possible that the accuracy of anticipated versus actual emotional reactions may be overestimated in this study compared with settings in which anticipated reactions are not explicitly addressed. Despite this potential difficulty, the likelihood of recall bias is limited by the prospective design of our study. Anticipated emotional reactions were assessed several months before result disclosure. Second, differences in periods of data collection for the p53 and BRCA1 testing programs might have reduced the comparability of information obtained, although the extent and direction of any biases are difficult to assess. For this reason, analyses were stratified by or controlled for testing program. Finally, the application of these findings remains limited by the relatively small number of participants in each program. Marginally significant differences must be interpreted with caution given the number of comparisons performed.

As genetic testing for cancer susceptibility finds its way into clinical medicine, it becomes crucial to define the optimal level of preparation for individuals contemplating testing. Other investigators have found that giving an individual time to "tell his or her story" or to muse on future scenarios seems to enhance adaptation after the actual event.²⁷ A psychologic intervention based on anticipation of subjective responses to BRCA1 or BRCA2 test results has been recently proposed to facilitate informed decisions about cancer predisposition testing.²⁸ It is hypothesized that giving patients the opportunity to rehearse their responses in role-play scenarios will attenuate or prevent unanticipated distress. Counseling in our and other cancer-predisposition testing programs has involved multiple sessions, each often several hours long. In contrast, when BRCA1 genetic testing is offered in the community and outside research protocols, one half of individuals report that the overall time allowed for counseling and discussion of informed consent is 30 minutes or less.²⁹ Ongoing randomized studies comparing the standard genetic counseling model with less intensive interventions may help to identify critical components of counseling.

Future research is needed to define which individual or familial qualities encourage adaptation and mastery by those undergoing genetic testing. Researchers are recognizing that the simple assumption that the test result itself would predict participants’ postdisclosure distress may not encompass the complexity of individual reactions to genetic testing. Smith et al²¹ reported that whereas change in mean distress scores of individuals tested for BRCA1 or BRCA2 did not differ significantly by test result, the variation in change in distress after disclosure was largely accounted for by consideration of the sex of the individual and his or her result in the context of the results received by other family members. Our study suggests that the ability to anticipate accurately one’s distress reactions to disclosure may be another predictor of psychologic outcomes after genetic testing. Identification of those at increased risk for heightened distress after disclosure will allow for targeting those individuals for further evaluation, counseling, and, in some cases, referral for psychologic treatment of distress. Cancer patients in particular may experience more distress than they anticipate. They and their providers may need to be alert to unexpected reactions to genetic information.

	ACKNOWLEDGMENTS

 
We are grateful to Frederick Li, MD, and Neil Klar, PhD, for their insightful discussions and other contributions to these projects. We also thank all of the family members and the genetic counselors who participated in these genetic testing programs.

	NOTES

 
M.D. is now with the Epidemiology Research Group, Department of Social and Preventive Medicine, Université Laval, Quebec City, Quebec, Canada

The p53 predisposition testing program was supported by the Starr Foundation, New York, NY, and by grant no. HG00725 from the Ethical, Legal, and Social Implications Program of the Human Genome Project, Bethesda, MD. The BRCA1 predisposition testing program was supported by grant no. HG12044 from the National Institutes of Health, Bethesda, MD. M.D. was a Terry Fox Research Fellow from the National Cancer Institute of Canada.

	REFERENCES

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Submitted July 6, 1999; accepted January 24, 2000.

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