Patient Perception, Preferences and ParticipationExploring the short-term impact of DNA-testing in breast cancer patients: The counselees’ perception matters, but the actual BRCA1/2 result does not
Introduction
Genetic counseling has been described as ‘the process of helping people understand and adapt to the medical, psychological and familial implications of genetic contributions to disease’ [1]. This assumes that genetic counseling influences the counselees’ lives, such as in their understanding and adapting to their possibly heritable disease. Many studies have indeed described changes in the counselees’ lives. For instance, after the communication of DNA test results for hereditary breast and ovarian cancer (i.e. BRCA1/2 genes [2]), some counselees decided to change the frequency of surveillance of breasts/ovaries and/or underwent prophylactic mastectomy or bilateral salpingo-oophorectomy (BSO) [3], [4], and some experienced distress [5], [6], [7], [8], [9], [10], [11].
The majority of follow-up studies have addressed the impact of genetic counseling and test results, whereas only a few have explained how genetic counseling leads to the observed changes. Explanatory studies are important to help understand why genetic counseling sometimes has a negative impact on counselees (e.g. [12]), and may support counselors in optimizing ‘the process of helping’ [1]. We therefore developed an explanatory model, which we will describe based on a short literature overview, and giving references as examples of general trends. We went on to empirically test our model. We focus on BRCA1/2 testing in cancer patients, because they are the majority of counselees who have DNA testing in the Netherlands but they are relatively understudied [10], [11].
Many studies have described the general impact of BRCA1/2 testing on distress and medical decisions in counselees (see model 1, Fig. 1). Most showed that different DNA results are associated with different outcomes. A pathogenic mutation (PM) result implies a high cancer risk for the counselee and a high likelihood that cancer is heritable in the family; after learning of a PM, many counselees decide to undergo frequent surveillance and/or prophylactic surgery of breasts and/or ovaries [3], [4], and feel somewhat distressed [6]. An uninformative result (UR) implies that no mutation was found but that the counselee's pedigree suggests that cancer is likely to be heritable in this family and the counselee is at increased risk of developing cancer (again); this result is associated with infrequent surveillance behavior and little distress in counselees [3], [4], [6]. An unclassified variant (UV) or variant-of-uncertain-clinical-significance is a genetic mutation for which the meaning is not known yet, i.e. it could be pathogenic or non-pathogenic, but the pedigree suggests heredity and high cancer risks for the counselee; this result is associated with many feelings of uncertainty, relatively high distress and the decision to undergo prophylactic surgery [13], [14].
These studies reported small to moderate associations between the communicated DNA test result category (PM, UR, UV) and outcome variables. They were followed by prediction studies in which the authors tried to explain how genetic counseling predicts outcomes. For instance, they predicted the impact from other information communicated by genetic counselors, i.e. the counselees’ cancer risks. Both the DNA test result category and the cancer risks do not seem to consistently and directly explain the medical and psychosocial impact of DNA testing [4], [5], [8], [9], [10].
Not finding a clear, direct relationship between the genetic information actually communicated and the outcomes caused previous researchers to look at the counselees’ perception of the BRCA1/2 results (model 2, Fig. 1). Several studies have described how about half of all counselees have an inaccurate perception of the communicated cancer risks [15], i.e. their perception was not in line with the genetic counselor's message. Subsequently, their – often inaccurate – perception influences their medical decisions and distress [7], [16], [17].
However, there is a large variance in the reported perception variables and effect sizes [15], [16], [17]. This may be because the counselees’ perception is a multidimensional construct [18], [19], [20], which has often been measured by only asking counselees about their recollection of their own cancer risk, and not, for example, of their relatives’ risks or likelihood of heredity [21]. Moreover, most counselees were asked about their recollections of the factually communicated genetic information, and not about how they interpreted it [19], [21], [22], [23]. The latter aspect involves subjectively selected, weighed and evaluated information, provided with personal meaning [21], [24], and seems to better reflect the counselees’ subjective construction of their risk perception than their recollections, because many authors have suggested that counselees subjectively interpret the cancer risks by using heuristics, such as their own beliefs about inheritance, past experiences with cancer in the family, subjective motivations, social comparison, and need for control [16], [25].
Our retrospective study [14] was the first to show that the counselees’ recollections and interpretations of their own cancer risks and heredity likelihood strongly predicted their long-term medical decisions and psychological well-being (see model 3, Fig. 1). Neither the DNA test result category that was actually communicated nor the counselees’ own cancer risks predicted any outcomes directly. The exceptions were PM results, which predicted the counselees’ decision to undergo prophylactic surgery; this could be because prophylactic surgery is usually only performed in the Netherlands after detecting a PM [14]. Our earlier study could be criticized for its retrospective design, which may have caused recall bias and relatively low reported distress, so in this empirical study we measured the short-term impact (Fig. 1).
The recollection/interpretation model in our previous studies was still a simplification of the reality of genetic counseling, in which more variables may be included in different parts of the model (model 4, Fig. 1).
Previous studies included the DNA test result category and/or the counselees’ cancer risks as predictors of the outcome of genetic counseling. In reality, counselors also often report the likelihood that cancer is heritable in the family (i.e. heredity likelihood [21]), the cancer risks for relatives, and the medical options (i.e. surveillance and/or surgery for breasts and/or ovaries), in line with Dutch counseling guidelines [26], [27]. They may also explain more about genetics (e.g. ‘future research may show a pathogenic mutation in as yet unknown genes’), and may report the risks in many different ways, such as describing the risk verbally or giving percentages [28], [29], [30]. Table 1 shows the possible pieces of information that can be communicated by Dutch counselors. All these subtle pieces of information may contribute to the counselees’ perception and the impact of the genetic counseling. It is therefore quite understandable that previous studies that included only one or two predictors, did not strongly predict the outcomes.
The counselees’ recollections and interpretations of their heredity likelihood did not strongly predict their distress in our retrospective studies [14]. This may be explained by the long time that had passed since the DNA testing was performed in our previous study, by the fact that ‘heredity likelihood’ was too abstract for the counselees to understand, and by the cancer risks of individual relatives probably being more relevant. The current study therefore included recollections and interpretations of the relatives’ cancer risks over a relatively short period, i.e. 3 months.
Previous studies showed that genetic counseling has a relatively small impact on the lives of counselees, possibly because of the relatively small range of impact measures used that had an insensitive or non-validated nature [31], [32]. The outcomes of genetic counseling may be more strongly predicted if genetic-specific instruments are used to measure how the counselees’ lives have changed [13], and how they experience vulnerability, mastery, and stigma related to heritable cancer [33].
Previous studies have been criticized for not taking into account the context of genetic counseling [11], [34]. The counselees’ medical history of cancer [3], [10], [11], [35], [36] and several sociodemographic characteristics – e.g. whether they have children – may influence their perception and outcomes [37], [38]. The familial context may influence perceptions and outcomes, e.g. the communication style within the family, cancer experiences in the family [38], [39], [40], [41] and the reason to undergo DNA testing (for themselves or relatives) [42]. The psychological context may also influence perceptions and outcomes, e.g. the counselees’ coping styles, cognitive representation of cancer and their personality [37], [38], [43], [44].
Our previous studies suggested that the counselees’ recollections and interpretations play a crucial role as mediators between the information actually communicated and the outcomes [14], [21]. We assume that recollections and interpretations are important because they represent the fundamental ‘process of flexibly integrating the communicated genetic information into the general context of their life’ [45]. We therefore hypothesize that both the information actually communicated and the contextual variables influence the recollections/interpretations, and indirectly influence the outcomes via – and only via – the complete mediation of recollections/interpretations. We expect the strength of the causal relationships between the recollections/interpretations and the outcomes to differ between the category of DNA result (PM, UR or UV), as suggested by the simple input–output models [3], [4], [6] (i.e. moderated mediation [46], see dotted line in model 4, Fig. 1).
In this explorative study, we wanted to predict the short-term outcome of giving a DNA test result to counselees who had already had cancer, by using an extended model (Fig. 1). We wanted to determine if the short-term outcomes of reporting a DNA test result are only directly predicted and/or completely mediated by the counselees’ recollections/interpretations? That is, can these outcomes be directly predicted by the DNA test result actually communicated and the contextual factors?
Section snippets
Sample and procedure
Eligible participants were women with breast and/or ovarian cancer who had requested a BRCA1/2 test in the period 2006–2009 at the Departments of Clinical Genetics of Leiden University Medical Center, Maastricht University Medical Center, University Medical Central Groningen, Erasmus Medical Center Rotterdam, or the VU Medical Center Amsterdam. All these centers offer genetic counseling according to Dutch guidelines, although this did not prevent some variation (see Table 2).
Eligible counselees
Description
467 counselees filled in the first questionnaire after the intake session (T1), and 248 (54%) of them returned the second questionnaire after the DNA test result (T2). At T1 decliners showed more negativity, worries, coped more often by denial and taking drugs (all d's = .2), and recalled a lower own cancer risks (d = .4).
The mean time since cancer diagnosis was 5 years; 94% had had breast cancer and 6% ovarian cancer. Metastases were detected in 26% of them. Before DNA testing, 56% had undergone
Conclusion
This study has confirmed [14], [21] the crucial role of the counselees’ perception, that is, their recollections and interpretations of the communicated cancer risks for themselves and for their relatives, and of the likelihood of heredity being involved. These perception variables were influenced by both the genetic information actually communicated, and the medical, familial and psychological context of the counselee. Subsequently, these perceptions predicted the counselees’ medical
Statements
We confirm all patient/personal identifiers have been removed or disguised so that patients and persons are not identifiable and cannot be identified through the details of the story.
Acknowledgement
We thank the Dutch Cancer Society for their financial support of this study.
References (76)
- et al.
A systematic review of perceived risks, psychological and behavioral impacts of genetic testing
Genet Med
(2008) - et al.
What is the impact of genetic counselling in women at increased risk of developing hereditary breast cancer? A meta-analytic review
Soc Sci Med
(2002) - et al.
A literature review of the psychological impact of genetic testing on breast cancer patients
Patient Educ Couns
(2006) - et al.
Predictors of perceived breast cancer risk and the relation between perceived risk and breast cancer screening: a meta-analytic review
Prev Med
(2004) - et al.
Putting it all behind: long-term psychological impact of an inconclusive DNA test result for breast cancer
Genet Med
(2008) - et al.
Experience of parental cancer in childhood is a risk factor for psychological distress during genetic cancer susceptibility testing
Ann Oncol
(2006) The construct validity of Ryff's scales of psychological well-being and its extension with spiritual well-being
Pers Individ Differ
(2004)- et al.
Interventions to improve risk communication in clinical genetics: systematic review
Patient Educ Couns
(2008) - et al.
A new definition of genetic counseling: national society of genetic counselors’ task force report
J Genet Couns
(2006) - et al.
The emerging landscape of breast cancer susceptibility
Nat Genet
(2008)
Genetic counselling and testing for inherited gene mutations in newly diagnosed patients with breast cancer: a review of the existing literature and a proposed research agenda
Breast Cancer Res
Psychological consequences of predictive genetic testing: a systematic review
Eur J Hum Genet
Emotional distress following genetic testing for hereditary breast and ovarian cancer: a meta-analytic review
Health Psychol
Psychological outcomes and risk perception after genetic testing and counselling in breast cancer: a systematic review
Med J Aust
Psychological impact of genetic counseling for familial cancer: a systematic review and meta-analysis
Fam Cancer
Psychological impact of genetic testing for cancer susceptibility: an update of the literature
Psychooncology
Adaptation to living with a genetic condition or risk: a mini review
Clin Genet
The counsellees’ view of an unclassified variant in BRCA1/2: recall, interpretation, and impact on life
Psycho-Oncology
A systematic review of the impact of genetic counseling on risk perception accuracy
J Genet Couns
How risk is perceived, constructed and interpreted by clients in clinical genetics, and the effects on decision making: systematic review
J Genet Couns
Risk as analysis and risk as feelings: some thoughts about affect, reason, risk, and rationality
Risk Anal
Feeling at risk: how women interpret their familial breast cancer risk
Am J Med Genet A
Why (cancer) risk communication can be hard
J Natl Cancer Inst Monogr
Perceiving cancer-risks and heredity-likelihood in genetic-counseling: the analysis of the counselees’ recollections and interpretations of BRCA1/2-test results
Clin Genet
Personal theories of inheritance, coping strategies, risk perception and engagement in hereditary non-polyposis colon cancer families offered genetic testing
Clin Genet
Meaning in the context of stress and coping
Rev Gen Psychol
Cancer risk elicitation and communication: lessons from the psychology of risk perception
CA Cancer J Clin
What clinicians can offer: assessing and communicating probabilities for individual patient decision making
Horm Res
Design of the BRISC study: a multicentre controlled clinical trial to optimize the communication of breast cancer risks in genetic counselling
BMC Cancer
Measurement of psychological factors associated with genetic testing for hereditary breast, ovarian and colon cancers
Fam Cancer
Methodology in longitudinal studies on psychological effects of predictive DNA testing: a review
J Med Genet
The development of a self-concept scale for BRCA1 and BRCA2 carriers
Psycho-Oncology
What do ratings of cancer-specific distress mean among women at high risk of breast and ovarian cancer?
Am J Med Genet A
Long-term psychological impact of carrying a BRCA1/2 mutation and prophylactic surgery: a 5-year follow-up study
J Clin Oncol
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