Communication about hereditary cancer risk to offspring: A systematic review of children's perspective

The present review describes how children experience hereditary cancer risk communication within the family.


| BACKGROUND
Hereditary cancer syndrome is a type of inherited disorder in which there is a higher-than-normal risk of certain types of cancer. 1 Most genetic syndromes involve autosomal dominant genes, but can also be recessive or de novo, and therefore, inherited and passed down from parent to child. Genetic susceptibility tests can identify specific mutations associated with specific hereditary cancer syndromes and tell if a family member has inherited the same mutation as other members who carry a cancer-associated mutation. 2 However, not everyone who has the mutation will necessarily develop cancer, even if the cancer-predisposing mutation is present in the family. 3 This process of identifying and assessing the hereditary cancer risk is completed through genetic counseling (GC), where health professionals support individuals in managing hereditary cancer risk. 4 Once genetic risk information (GRI) is distributed among family networks, the moment of becoming aware of the increased susceptibility to cancer can be a disturbing event, both at personal and family levels. [5][6][7] Growing up in a family with known hereditary cancer risk may involve additional psychosocial burden and be challenging.
For instance, when a child is affected by an inherited genetic condition, unaffected siblings can subjugate their feelings and needs and may isolate themselves when coping with it. 8 The impact of hereditary cancer risk information on children, affected or not affected, should not be underestimated. While prior research has contributed to our understanding in how adults perceive, react to and adjust to cancer risk information, there continues to be a need for further research that sheds light on what it means for a child to live in a family affected by hereditary cancer syndromes. 9 Previous systematic reviews demonstrate agreement between professionals and parents in the role that parents have in being primarily responsible for discussing family genetic information with their children. 9 Also, children have reported their preference for being informed about an existing genetic condition in their family. For example, children from families with a recessive genetic condition reported being curious and demonstrate the ability to assimilate information from a young age. 10 Likewise, children from families affected by Huntington's Disease, a genetic inherited condition, in a retrospective study expressed a preference for early disclosure and open communication in the family. 11 In families with hereditary cancer risk, children have reported feeling upset and frustrated with family secrecy about the disease, which contributed to tense relationships between family members. 9 Families also emphasize the importance of open communication, and report feeling empowered when they openly talk about the condition as it facilitates discussion on concerns as they arise, and reinforces mutual support and care for each other. 9 Emotional impacts can vary and be experienced as negative or positive in relation to receiving genetic information.
When open communication exists, young people may mature into adulthood with a cautious mind regarding reproduction and genetic testing decisions, which can empower their own choices and psychological health. In contrast, poor communication has been associated with less optimal choices and emotionally-driven decision-making. 9 Overall, providing information, checking understanding along the way, and explaining and managing the emotional feelings as they emerge seems to be integral to support children's coping with GRI. 9 Thus, communication affects how information is received and has implications for psychological adjustment for the child. 12 A key finding noted in the literature is that parents are challenged with what and when to tell their children, and have different concerns and questions depending on their children' ages. 9,13,14 A major concern is the extent to which information about hereditary cancer risk affects a child's psychological well-being and development. Two systematic reviews and meta-synthesis synthesized existing evidence on family communication to at-risk relatives for hereditary adult-onset cancers and the support required for parents and children to manage the genetic condition or the risk. 9 into Excel and reviewed for relevance, and the full-text articles were reviewed for inclusion and data extraction. All titles and abstracts of the identified studies were independently assessed by two authors for inclusion or exclusion in the review, until a good level of agreement was reached (97%). The inclusion and exclusion criteria were based on the population, concept, and context of the research question (see Table 1). In particular, we included studies with samples of minors (<18 years old), or adults who were retrospectively describing their experiences as minors ("retrospective children").
Papers were excluded when all reviewers agreed that inclusion criteria were not met and disagreements were resolved by discussion to reach consensus. Eleven (1.6% of 695 eligible abstracts) studies met all of the inclusion criteria, and four additional studies were identified through other sources. The eligible papers were assessed for quality using the Mixed Methods Appraisal Tool (MMAT 19 ). Two independent judges responded "Yes", "No" or "Can't tell" to the screening questions according to the MMAT checklist, depending on the appropriate category of the study appraise (see Appendix B). The included studies were of relatively high quality: 80% had clear research questions, and 93.33% addressed them by the collected data. Ninety-eight percent of the qualitative and 96% of studies with mixed-method methodology were of good quality (see Appendix B).
Finally, two independent researchers extracted information from the included articles using tables that recorded study outcomes, study design and the main findings (see Table 2). We then compiled all the information for each topic and summarized the results according to the research questions they addressed.

| Available literature
The search returned 15 articles (see Table 2) that met the inclusion criteria (see Table 1

Include Exclude
Population Children as minors-affected and siblings (<18 years old).
Only parents referring to their children.

| How, when and what is discussed about hereditary cancer risk in the family?
Information regarding "who" provided the disclosure of the genetic condition to the child was present in only six (40%) of the selected studies. For the most part, children indicate that they came to know about the genetic risk in the family through their mother. Parents typically shared the test results alone, or with their spouses. In some cases, the offspring's siblings or other family members were present during disclosure. Offspring tended to learn GRI either in a nonformal family meeting, for example, by telephone or while engaged in another activity such as driving in the car, 20 or through a more intentional private conversation (see Table 3). 20 counselors about test results, risk management, hopes, and fears.
In relation to the age of the child at the time of disclosure, the youngest age of an offspring learning of a genetic test result was reported as being 8 years old. 23 Only one study indicated the specific age at the time of disclosure, 24 while the remaining selected studies used age categories (e.g., "> 13 years old", "12-15 years old", etc.), or developmental stages (e.g., "teenager", "emerging adult", etc.). The most common estimated age categories of offspring at disclosure  ranging from hours to a few days following disclosure to the family member, 20 to years. 24,25 Among the young adults who reported retrospectively, they expressed difficulty in recalling the length of time between when they received information from that of their parent learning of a test result. 20 Information regarding the content of disclosure was present in only four (26.67%) of the selected studies. In some cases, the specific genetic mutation itself was not described, although the parents did discuss the hereditary risk of cancer in the family. The most frequently reported information when disclosing to children was content concerning the implications of the test result for the risk of developing cancer-"He [dad] said that testing had been done on his side of the family and a gene was found that makes women prone to breast cancer (…)" 24 (see Table 3) -and the eligibility of the offspring for genetic testing. Risk reduction strategies (cancer screening, prophylactic surgeries, and avoiding tobacco) were a less frequent topic of discussion at the time of disclosure. 24 However, the disclosurerelated content can vary depending on the age of the child or depending upon the preventive/current health activities of the parent. For example, disclosure of the mother's BRCA1/2 mutation status to daughters was sometimes conflated with the news that the mother would shortly be undergoing preventive surgery. 20 For children <11 years old, information tended to focus on events that the child would witness (e.g., hospitalization of a parent). For younger age groups, parents tended to use simplistic language to describe breast cancer: "poorly boobs", "poorly tummy", "magic medicine", "new boobies", "boob job". 21  The included articles only sometimes provided all the information regarding the participants.

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-LIMA ET AL. children reported feeling "relief" and being "glad" about the information, both in terms of their own health and in relation to that of their mother's. When a positive test result was received by a parent, children may also experience a favorable reaction that appeared to be due to the empowering nature of the knowledge that the test result provides in relation to health prevention strategies, treatment options, and future plans. 12 The negative responses to disclosure among offspring included feeling apprehensive about their own future health and that of their mothers'-"I was nervous for her [mother] more than myself right away (…)" 20 (see Table 4). Some cases of dispassionate and neutral responses to the disclosure process were described as children simply feeling "not surprised by the news". 12 When having siblings, on the one hand, young adults reported feeling guilty when a close sibling tested positive (and they don't carry a mutation)-"A feeling of guilt that I don't have it (…)" 26 (see Table 4). On the other hand, children can also feel closer to their siblings as they experience having something in common-"It probably brought me and my sister closer together (…)" 26 (see Table 4). Young adults who received genetic information often expressed having the responsibility to inform younger siblings and cousins, so that they obtain accurate information. 22 Although the majority of children articulated thoughts and feelings about how they wanted parents to communicate over time with them about a hereditary risk, children did not always engage in family communication in follow-up with their own parents, as they often had difficulty articulating their feelings. Some children reported that they did not address their own stress/anxiety, even when recognizing concerned others would support them-"(…) I had a sense of I need to not make people think that I'm scared of things (…)" 12 (see Table 4).
Younger children reported that they wished to avoid negative feelings. 12 Children's psychological adjustment may be related to their beliefs about health and thoughts of illness. For example, children with more psychological symptoms experienced more frequent thoughts of becoming sick, about developing cancer, and had worries about cancer developing in a family member. 27 Some studies indicated that the testing results have had no impact on family relationships, 26 within or outside the family. 24 However, one study found that sadness and social isolation could be triggered by watching older family members die from the same disease. These participants described a void related to familial mentoring relationships-"(…) I wished I had a woman there I could talk with (…)" 28 (see Table 4).  Table 4). The authors in this paper also indicated that partial  Table 4). In another study on HBOC families, children reported on important reasons for testing (when reaching adulthood), which included (in order of importance): to pay closer attention to one's own health; to make more informed decisions about family; to feel better; to make better decisions about smoking or using tobacco; to plan for school or work. 27 Genetic testing in general was reported as having the advantage of allowing opportunity for efforts in disease prevention, supporting living a healthier lifestyle through health preventive behaviors (e.g., exercising regularly, eating a healthy diet and avoiding tobacco), and engaging in early screening for disease detection and treatment 24,26 (see Table 4). However, age was often experienced as a barrier to addressing cancer risk as children reported being told that they were too young for conventional screening measures. Some young adults described feeling pressured by their parents to act before reaching a certain age perceived as being unsafe, as a sense of urgency in risk management. 29 -881 syndromes and/or testing initially and revisiting the topic over time was deemed very important. 12,23 Open communication was valued in six (40%) of the selected studies. Children described preferences in parents communicating the information honestly in a way that is reassuring, with less potential to frighten the child-"(…) I'd rather know the full truth" 23 (see Table 5). Children also identified tone as being relevant. 23 Regarding the involvement in testing decisions and the satisfaction with it, adolescents and young adults reported that they had received enough input concerning information on the decision-making process within the family. Children stated that they trusted their parents' judgment, as having their best welfare in mind 26 (see Table 5).

| Professional care
A key theme identified in the review was that children have interest in knowing, as future adults, about their risk for developing cancer. 27 In all studies, offspring showed interest in learning more about genetics and hereditary disease. In one study, quantitative data demonstrated an average of 9, on a scale from 1 to 10, indicating the need for information. 30 Despite 12 studies (80%) reporting that the family attended GC, only one study indicated that the children were included in the service. 31 Qualitative and quantitative findings showed that young adults who received GC expressed satisfaction with the care that they received, and when participants indicated that they were not satisfied, this was related to the experiences associated with a lack of continuity of care. Continuity of care was especially valued-"(…) It's almost like they [genetic professionals] are a family member" 31 (see Table 5). Some young adults indicated that GC 29,31 and multi-family discussion groups 32 had prompted debate among family members concerning the implications of knowing about a hereditary condition in the family.
Children and young adults reported a perception of guilt being experienced by their parents for passing the mutation on to them. 12,22,29 With this experience, when there were joint GC sessions (with parents), young adults reported a tendency to hide their worries, denied concerns, or refrained from asking critical questions about the implications of their mutation status, their cancer risk, or on methods of risk reduction, in an attempt to protect their parents from potential additional burden and emotional distress. 29 Children expressed being aware that their mothers were putting on a "brave face" and felt that by asking questions they may cause upset to their mothers. 21 Only four (26.67%) studies described using tools (e.g., written materials, professional journals, or the internet) to support the disclosure process. Offspring who received written materials indicated that they found the information helpful. Among offspring who did not receive written materials, the majority felt that written materials would have been helpful, either for themselves or for others.
Offspring also suggested value in having opportunity to meet with a genetic counselor or other health professional. 22,24,31 Regarding testing, there are reports from sons and daughters supporting the genetic testing of minors for adult-onset syndromes 26,30,33 -"It should be their choice (to test). We should leave it open to people" 33 (see Table 5). Among offspring who expressed caution against testing of minors, the primary reason identified was the lack of medical indication for children. 33 In relation to the recommended age for genetic testing, various recommendations were offered. For example, in one study on HBOC and Lynch syndrome: 2% of the participants suggested from birth, 4% suggested starting at 16 years, 24% starting 18 years, 20% from 20 years, 18% from age between 21 and 24 years, 18% from 25 years, and 2% from 30 to 35 years; 12% did not report a recommended age for testing, stating that it depends on the person. 30 Overall, this review found that there was no strong agreement in terms of the age preferences for testing, although we note that the studies included did not specifically consider this topic, regarding either adult-onset versus youth-onset disorders. Adult-onset and youth-onset conditions differ in relation to the age eligibility for genetic testing.

| DISCUSSION
This is the first systematic review of children's experiences and preferences regarding communication about hereditary cancer risk within the family. Results confirm that disclosure of genetic information is usually performed by parents, and children explicitly indicate that this is their preferred way to learn that there is genetic cancer risk in their families. In the reviewed studies, the person disclosing was typically the mother, which is in line with previous findings indicating that women often take on the primary role in disclosure and act as family "representative", "kin keeper", 34 or "gatekeeper". 35,36 Children didn't report preferences regarding the method of disclosure, either in a formal or informal way. However, they may be particularly sensitive to their parent's emotional state.
When children perceive their parents as being uncomfortable, distressed, or not giving space for questions, communication about genetic risk can be hindered. Children may hide their worries and anxiety, or refrain from asking questions (despite wishing for more information), to protect a parent from additional emotional distress.
Dynamics of "protective buffer" have been described between the couple, or from parents toward their children, in families affected by genetic cancer syndromes. 6   This can be a difficult task for parents, particularly among those who are emotionally affected themselves by the genetic information and who may feel unprepared in how or what content specifically to provide to an offspring member of their family.

| Clinical implications
Our findings have implications for GC and psychosocial care. Genetic counseling and other health professionals can provide support and psychoeducational guidance, which is crucial to support parents to cope with and manage their own personal feelings and experiences through the disclosure process 13 The literature recommends follow-up visits or appointments with a psychosocial specialist to discuss potential impacts of cancer/risk knowledge, the progress of family communication, 38 and to support adaptation to new information. 9 Our findings showed that offspring directly expressed a need for accurate information regarding ge-

| Study limitations
One limitation of this review is that it provides little information about the perspectives and experiences around genetic testing for cancer from offspring across various cultures. We could only identify 884 -Kingdom, and Australia), addressing mostly two genetic cancer syndromes (HBOC and LFS). Cultures are known to vary in relation to family belief systems and values which may impact responses and adjustment to genetic information, 34 so further international studies are needed. Another limitation of this review was the small number of studies with only children as participants, which informed our decision to also include studies with adult offspring who retrospectively reported on their experiences as children (when they were <18 years old). Thus, our review relies on the inclusion of data sustained by a few articles. The experiences described by offspring may have altered over time, leading to a different meaning as people enter adulthood and assimilate information over developmental life stages.
Not including parents' perspectives in this review also limited the scope of admissible studies. Furthermore, we also were unable to find studies that investigated families who decided not to disclose GRI to offspring. A family is a system and in not having every member's perspective (which may differ) and across various situations (e.g., in families choosing not to disclose GRI to offspring) calls for caution about the generalization of these findings. We note that we also included papers with multiple goals and that did not specifically focus on minors' experiences of being in an at-risk family. Finally, it is important to note that we included studies with samples that involved both pediatric and adult-onset syndromes. This is an important limitation to note, as the age eligibility for genetic testing differs between that for early onset versus an adult-onset disorder.
We were unable to ascertain differences between the types of disorders in relation to specific offspring reactions. Offspring are open to, and have a preference for being included in the GC processes to address issues concerning their own potential cancer risk, even before the recommended age for genetic testing.

| CONCLUSIONS
Findings point to the relevance of a family-centered care in hereditary cancer risk that targets not only the mutation carrier individually but also their children and partners.

ACKNOWLEDGMENTS
This work was funded by the Portuguese Foundation for Science and Technology (FCT) (grant EXPL/PSI-GER/1270/2021).

CONFLICT OF INTEREST STATEMENT
We have no known conflict of interest to disclose.

DATA AVAILABILITY STATEMENT
The data that supports the findings of this study are available in the supplementary material of this article.