Breast cancer (BC) is a major public health concern for women, with almost 1.7 million new BC diagnoses worldwide in 2012 [1
]. Among these BC patients, 10% to 20% present with a BC family history, and two decades ago, BRCA1
were identified as major BC susceptibility genes [2
]. Women who carry a mutation in the BRCA1
gene face up to a 72% and 44% risk of developing breast or ovarian cancer, respectively, by the age of 80 [3
]. When already affected with BC, these women present an increased risk of contralateral BC [3
The identification of a pathogenic variant in highly penetrant genes such as BRCA1
provides options for early detection or prevention. There is evidence that a risk-reducing bilateral mastectomy decreases the risk of BC by 85% to 100% [4
], and that risk-reducing bilateral salpingo-oophorectomy reduces the risk of ovarian cancer by 69% to 100%, and the risk of BC by 37% to 100% [4
]. When a pathogenic variant is identified, genetic testing may be offered to relatives.
Recently, additional genetic factors have been identified, including rare variants with “moderate” (CHEK2, ATM, BARD1
) to “high” (PALB2
) BC risk [5
]. Thanks to technological advances, instead of testing the BRCA1
genes alone, panels of genes may now be simultaneously tested, at a reduced cost and faster turnaround [6
]. As a result, over the past few years, these tests have entered oncologic genetic clinics [7
National guidelines recommend the inclusion of cancer genetic testing within a framework of genetic counseling [10
]. This healthcare discipline is defined as “the process of helping people understand and adapt to the medical, psychological, and familial implications of genetic contributions to disease” [11
]. Among tasks such as cancer risk assessment, informed consent collection, the disclosure of genetic test results, and medical recommendations, genetic counseling comprises psychosocial assessment [12
]. Thus, the relevance of a ‘patient-centered care approach’ addressing psychosocial needs in this clinical setting should be underlined.
Psychosocial needs refer to psychological and social difficulties, and the type and extent of help a patient actually needs or expects in order to manage these difficulties [13
]. Potential needs in cancer genetics may be motivated by specific issues related to the cancer genetic risk, counseling, and testing [14
], and may request additional help from a clinical geneticist, genetic counselor, gynecologist, breast surgeon, or psychosocial worker. In past decades, there has been increased interest in needs assessment in cancer care [15
], and in cancer genetics; specific questionnaires have been developed in order to address these concerns and adjust cancer care as necessary [16
Genetic counseling confronts large quantities of information involving statistic and genetic concepts, which are generally imprecise and complex, and are sources of uncertainty [18
]. Moreover, genetic counselors tend to communicate unidirectionally, providing large pieces of information, and at the same time often neglecting to enquire about counselees’ needs [19
], leaving them with potentially unfulfilled needs after the consultation [20
In the gene panel testing environment, genetic counseling is further complicated, as information must be provided on possible new quantitative results (i.e., “moderate” cancer risk with unwell defined guidance for clinical management [22
]), an increased number of variants of uncertain clinical significance (VUS) [23
], or the possibility of secondary or incidental results [24
]. In addition, the involvement of non-genetic factors in BC risk [25
] further complicates counseling.
Assessing psychosocial needs during the care trajectory allows for clarifying what type of interventions (i.e., depending on specific needs) or for which population (i.e., depending on its characteristics) the provision of specific health care resources is necessary [26
]. Variations across countries in the BC genetic risk counseling process exist, e.g., in terms of risk communication [27
] or clinical recommendation [22
]. Patterns of psychosocial needs are expected to vary according to these variations.
Psychosocial needs may also reveal based on counselees’ sociodemographic, family history, and clinical or psychosocial characteristics. If their psychosocial needs are similar across counselees’ characteristics, but are different across countries, this implies that the mode of counseling delivery is associated with needs, and this may have implications for clinical practice according to specific settings [28
To our knowledge, only two United States (US) studies [29
] reported on psychosocial outcomes in women at high genetic risk of BC undergoing gene panel testing. Initial (pretest) genetic counseling generally provides information allowing counselees to make informed decisions regarding testing and the receipt of genetic information. The present study addressed the psychosocial needs of women at a high genetic risk of BC undergoing genetic counseling in French and German cancer genetic clinics in order to highlight possible unmet care needs before actual genetic panel testing.
Specifically, we aimed to:
Assess the prevalence of moderate and high psychosocial needs in women undergoing genetic counseling and testing for BC risk in a French and a German cancer genetic clinic, and compare them between the two countries;
Explore sociodemographic, clinical, psychological, and geographical (i.e., the country setting) factors associated with the number of moderate and high psychosocial needs in these women; and
Compare these results with empirical data extracted from a literature review addressing the domains and specific items of psychosocial needs that are most frequently reported along the cancer genetic counseling and testing process.
2. Materials and Methods
This study protocol was approved in France by the Comité consultatif sur le traitement de l’information en matière de recherche dans le domaine de la santé (CCTIRS: Consultative committee for information management in health research—No. 16.314, France), and by the Commission Nationale Informatique et Libertés (CNIL: French Information Technology and Privacy Commission), and in Germany by the Ethics Committee of the University Hospital of Cologne. All of the recruited women provided written informed consent.
2.1. Participants and Procedure
From October 2016 to July 2017, women over the age of 18 years, who were either healthy or affected with a primary non-metastatic breast cancer, and eligible for BC gene panel testing, were consecutively recruited at the cancer genetic units of the Institut Curie (Paris, France) and the University Hospital of Cologne (Cologne, Germany). A minimum sample size of 200 was required to allow for comparisons between the two country cancer genetic services. Women with a recurrent BC, a personal history of ovarian cancer, or a major psychiatric disorder were not included.
The study objectives were explained to the women on the day of the initial cancer genetic counseling visit, and when they agreed to participate, they were given questionnaires to fill in at home, either in paper or online, and to return within the next two weeks. Questionnaires not completed or received within 28 days after the genetics consultation were considered missing. If necessary, 14 days after the consultation, one reminder was made by telephone call.
2.2. Questionnaire and Data Collected
2.2.1. Psychosocial Outcome
The ‘Psychosocial Aspects of Hereditary Cancer’ (PAHC) questionnaire is comprised of 26 items organized into six problem domains, i.e., needs related to hereditary predisposition, practical issues, family and social issues, living with cancer, emotions, and children-related issues [17
]. Participants are asked to rate each question on a scale from “not at all” (1), “a little” (2), “quite a bit” (3), or “a lot” (4). A “not applicable” option is provided to some items (e.g., items regarding children-related issues). The PAHC items were translated and adapted into French and German according to international guidelines [31
], and were pilot tested in the respective country’s cancer genetic clinic. The internal consistency of the overall PAHC 26-item scale was 0.87.
2.2.2. Independent Variables
General distress (i.e., anxiety and depression) was measured by the Hospital Anxiety and Depression Scale. This scale comprises anxiety (HADS-Anxiety) and depression (HADS-Depression) subscales, and has French [32
] and German [33
Women were also asked if they had lost family member(s) due to breast or ovarian cancer.
To compute the objective risk estimates of breast and of ovarian cancer up to the age of 80 years, the Breast and Ovarian Analysis of Disease Incidence and Carrier Estimation Algorithm (BOADICEA) web application (BWA v3, University of Cambridge, Cambridge, UK) [34
] was used.
Additional data were collected on the sociodemographic characteristics provided by the patient, and the clinical data obtained from the medical record.
2.3. Statistical Analysis
Baseline sociodemographic and clinical characteristics of the participants were described using the mean (standard deviation) or median (range) for continuous variables, and the number (percentage) for qualitative variables. We used the Student t-test for quantitative data and the Chi-square test for categorical data to compare study participants among the French and the German respondents, and between the age of overall respondents and non-respondents. Response frequencies were computed for each PAHC item. We computed the frequency (percent) of individuals reporting moderate to high needs (at least “quite a bit” responses) per item. A Chi-square test was performed to compare the percentage of patients with a moderate to high need per item between the two countries.
Multivariate regression analyses were performed on the number of needs (rated at least “quite a bit”) per individual, as a dependent variable. Psychosocial needs were taken as a whole, considering that the PAHC structural validity was not yet confirmed in these PAHC language versions (work in process). The country sample, age, educational level (secondary school or below versus superior education), marital status (married or partnered versus single, separated, divorced or widowed), parental status (having children or not), HADS-anxiety and HADS-depression scores (continuous variables), health status (affected or not with a present or past BC diagnosis), and family history (having lost a blood family member from breast or ovarian cancer) were assessed as potential predictors in univariate analyses. The collinearity between variables was tested in univariate analysis; variables presenting collinearity were not simultaneously included in the same multivariate model. A stepwise selection approach was then used to select the final multivariate model.
2.4. Literature Review Procedures
A systematic search of the PubMed/Medline database was conducted. We selected papers published between January 2000 (before that time, BRCA1/2
psychosocial outcomes were mainly addressed on researched cohorts rather than in “real” clinical practice [35
]) to 17 October 2017 (last check), assessing the overall psychosocial difficulties or needs of women who had a high breast or ovarian cancer genetic risk, and considering only observational quantitative studies, using genetics-specific, multidimensional measures (keyword combinations, see Supplementary Materials Table S1
All of the titles and abstracts were inspected for relevance, excluding papers such as protocol descriptions, literature reviews, studies addressing the period of referral or following cancer risk management decision-making, men only, healthcare professionals, genetic testing for breast or ovarian treatment decision-making, or controlled (randomized) trials. Thirteen papers were rejected on full text as they only addressed a specific outcome (e.g., general or specific distress, quality of care perception) (11 papers) or generic difficulties/needs measures such as the SF-36 (two papers). The two remaining papers [36
] were analyzed in addition to five studies identified from a manual search [30
], for a total of seven inspected studies.
Two authors (Anne Brédart and Jean-Luc Kop) extracted the study descriptive data (study country, sample size, response rate, study population age and gender, timing of assessment, type of cancer genetic risk, cancer diagnosis status, and psychosocial need measure; see Supplementary Materials Table S2
), and the prevalence of needs (the number of patients that expressed individual need items), and identified significant relationships between the various factors and psychosocial needs within each study. Additionally, the psychosocial needs measured were described based on the original publication (which measured the aim and targeted population, number of items, scales/domains, developmental and psychometric information, and scoring method; see Supplementary Materials Table S3
This study primarily aimed to assess the prevalence of psychosocial needs in women initiating genetic counseling for high BC risk in a French and a German cancer genetic clinic, and explore correlates of increased needs, including the country setting. We compared these results to data extracted from a literature review in order to shed light on implications for research and clinical applications.
A substantial proportion of women in both countries perceived significant difficulties in the “living with cancer” domain, which referred to living with both actual cancer as well as the threat of personal or familial cancer diagnoses. In addition, they also experienced concerns in the “family and social issues” domain, representing the interpersonal aspects of the cancer genetic risk. Interventions should thus focus on these particular difficulties in both institutions. Besides, independently from the country, the overall number of needs was found to be higher in younger women, in those having children, or those presenting increased anxiety; therefore, attention should be given to the needs of these women in particular.
Specific differences were also observed between the two country samples. For instance, compared to the German sample, a higher proportion in the French sample worried about children-related issues. For example, women attending the French cancer genetic clinic more frequently expressed “guilt about the chance of passing on genetic alterations to their children” than the German sample; this may suggest that women in the French genetic clinic may need additional counseling for dealing with this feeling of guilt. In contrast, women attending the German cancer genetic clinic more frequently expressed preoccupations related to the hereditary predisposition, such as “worries about the choice of possible preventive options (screening versus surgery)”, which points to the need for additional support in decision-making with regard to management options in the German clinic.
Significant differences (i.e., education level, BC status) between the two country samples may require specific clinical implications by clinic setting. As only the actual BC diagnosis status appeared to be (to some extent) related to a higher number of needs, interventions should predominantly emphasize the needs of women affected with BC.
Our results are in line with the information obtained from the literature review, confirming a high prevalence of psychosocial needs following genetic counseling, including aspects in relation to the cancer diagnosis [40
] or family and social issues [38
] after the initial cancer genetic consultation.
Other reviewed studies investigated the prevalence of these needs over time, showing that these needs may remain high (above 50%), independent of the genetic test result: 59% of women worried about the “implications of being at increased risk of cancer for other family members” one month after the initial genetic consultation [38
]; 84% of BRCA
1/2 carriers and 69% of non-carriers “worried about their risk of getting cancer/again” [39
]; 57% of BRCA
1/2 carriers “dealt with fears about developing cancer” at about two years after the genetic test result disclosure [36
]; and 59% felt confronted with “uncertainty” about seven years after receiving the genetic test result [41
]. This underlines the importance of monitoring psychosocial needs over a longer period of time in individuals confronted with BC genetic risk.
The literature review data found that younger age [36
], having children [40
], and anxiety [39
] correlated with psychological needs, thus supporting our findings. To gain further insights into the psychosocial needs of women along the process of BC gene panel testing, we are currently planning a follow-up assessment on psychosocial needs after the women’s receipt of the genetic test result. In line with the literature, we expect significant differences between women according to the genetic test result received (positive, negative, or VUS) in terms of intensity [30
] or hierarchy [39
] of needs.
This report comprises a number of limitations. Our study samples mainly comprised BC patients; therefore, the results may not reflect the psychosocial needs of healthy women that are at a high BC genetic risk (e.g., female relatives) undergoing genetic counseling. Moreover, we assessed a limited number of needs correlates, thus potentially missing out on other relevant needs. Further, so far, our data is cross-sectional, i.e., no causal conclusions can be drawn. Hence, in order to provide more specific clinical recommendations, further research should address additional factors in longitudinal study designs. The impact of recent advances in BC risk genetic testing and counseling requires the monitoring of counselees’ well-being. Future research should address the effects of different genetic counseling delivery models, such as the risk communication style on counselees’ psychosocial needs.
Only two quantitative studies that addressed overall psychosocial needs were identified from the literature review based on the chosen databases and keywords. In fact, the psychometric assessment of needs happens to be a relatively new area of research in the cancer field [15
]. In the genetic counseling context, this outcome has hardly been considered [43
]. The development of a standard questionnaire to assess psychosocial needs in the cancer genetics population has only recently been implemented [17
Among the seven studies selected, the population samples varied (i.e., in terms of hereditary cancer syndromes, cancer diagnosis, gender, assessment timing), and so, beyond general observations such as high needs prevalence regarding the cancer experience or in relation to younger age and anxiety, making comparisons and drawing conclusions on more specific observations between studies remain problematic.
Moreover, four different needs questionnaires were employed. Most of them assessed the severity of difficulties, concerns or worries [38
], and positive or negative emotions [39
]. Only Farrelly et al. [36
] used a questionnaire that directly assessed the presence and intensity of needs, whereas only such an instrument can pinpoint the patient’s or counselee’s expectations with regard to counseling. Furthermore, the data obtained from these different questionnaires were reported in different ways (i.e., either item by item, or by domain or scale), and only one questionnaire (MICRA [16
]) evidenced psychometric properties.