INTRODUCTION

Genomic sequencing is becoming further integrated into clinical practice, leading to higher rates of molecular diagnosis of genetic conditions [1]. In many cases, findings from genomic sequencing are not only relevant to patients but also to patients’ families. When a pathogenic variant is identified in a patient, this finding may also indicate that another family member is at risk of either developing the condition, passing the condition on to their children, or both [2]. Family disclosure is important as relatives who are informed of their genetic risk can access testing, a process known as cascade testing. If they are found to be at risk or carriers of the condition, they can take measures to either prevent or better manage the genetic condition of interest, or make more informed reproductive choices [2]. Empirical research on family communication demonstrates that not all family members are informed of their genetic risk [3]; some family members may only realize they carry the pathogenic variant once they become symptomatic. A Dutch survey study found that more than half of patients found it burdensome to inform family members of their genetic risk [3]. The most common reasons that patients do not inform their family members relate to family conflicts and concerns that the genetic risk information will cause distress if disclosed [4]. To facilitate disclosure of genetic information, health-care professionals (HCPs) often provide patients with a family letter containing information regarding familial inheritance and options for testing to distribute to their family members [5]. Alternatively, HCPs may, in some cases, directly disclose genetic information to family members, either with or without the patient’s consent.

While some patients may explicitly refuse to inform their family members (known as active nondisclosure), more commonly, HCPs are unaware of whether patients passed on the information [6]. This is because while patients may agree, or at least not object, to inform their relatives when asked by their HCP, they do not always follow through in practice (known as passive nondisclosure). If a HCP learns that the patient did not inform their family members, they are faced with the challenge of balancing the interests of their patient with that of their patient’s family members. The HCP has an obligation to respect the patient’s right to confidentiality of their genetic information, but the HCP may also have a conflicting obligation to prevent harm in the family members by providing them with information about clinical and reproductive implications. While active nondisclosure only occurs in a small minority of cases, many HCPs encounter this dilemma over the course of their careers and feel uncertain about how to balance their responsibilities toward patients and their family members [7,8,9].

This uncertainty faced by HCPs is due in part to the lack of consensus on questions at the heart of this ethical conflict, such as the degree to which communication with family members is the responsibility of the patient versus that of the HCP, and what options HCPs have in the case of nondisclosure. This matter is further complicated because while in some jurisdictions professional guidance is supported by legislation, in others, guidance may not have corresponding legislation outlining obligations and protections. Legislation was beyond the scope of this review; however, it warrants consideration to better understand how guidelines may apply in particular jurisdictions.

To address these questions, we examined published ethical guidelines, policies, and recommendations to better understand how issues around family communication are currently addressed by normative documents. More specifically, we wanted to examine how they suggest HCPs should discuss and facilitate family disclosure, as well as how they address the ethical conflict in cases where the patient does not consent to disclosure. Although a review on this topic was performed in 2007 by Forrest et al. [10], with the integration of genomic sequencing into the clinic, the landscape has since changed and, as such, the issue bears re-examination.

MATERIALS AND METHODS

Search strategy

Our search for relevant normative documents involved three strategies. First, we performed systematic searches of PubMed, Web of Science, and Google Scholar using the following search string: ([guideline* OR policy OR report* OR recommendation* OR “points to consider” OR “position statement”] AND [family OR familial OR families OR relative*] AND [Communic* OR disclosure OR disclose OR disclosing] AND [genetic OR genomic)]. Second, we searched the HumGen database (HumGen.org). Third, we utilized a snowballing method, which involved checking the reference section of the retrieved documents for additional documents. The searches were conducted between January and March 2020 (summarized in Fig. 1, PRISMA flow diagram).

Fig. 1
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PRISMA flow diagram.

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Documents were eligible for inclusion if they (1) were normative documents, i.e., ethical or clinical guidelines, position statements, recommendations, or points-to-consider; (2) were issued by international or national level authorities; (3) were in English; (4) addressed the clinical setting (rather than solely research); (5) addressed health related information (rather than just paternity or reproductive implications, e.g., carrier screening). Date of publication was not restricted. Documents that focused exclusively on children or legally incapacitated probands, who cannot give consent themselves, were excluded. Initial screening for inclusion based on title and abstract was done by one researcher (A.P.). Documents where inclusion was unclear were discussed with a senior researcher (D.F.V.).

Data analysis

Relevant quotes were extracted from the documents and analyzed using a combination of deductive and inductive coding. First, deductive codes were developed by the research team prior to the document analysis based on a review of the literature [11]. Codes were added inductively during analysis of the documents. Coding was performed independently by two researchers (A.P. and D.F.V.); coding was compared, and all discrepancies were resolved through discussion.

RESULTS

Thirty-five documents met the inclusion criteria (see Supplemental material for full list of documents). Documents were published by national advisory committees from Australia, Canada, Denmark, France, Germany, Italy, Japan, the Netherlands, UK, United States, as well as at the European and international level. Publication dates ranged from 1991 to 2019.

Our analysis identified four main categories: (1) discussing family disclosure with the patient, (2) aiding family disclosure, (3) disclosure without patient consent, and (4) balancing rights and duties of family disclosure. Although presented in separate sections, it should be noted that documents discuss multiple categories and furthermore that these categories are not independent from each other, but rather have overlapping aspects. Illustrative quotes from the documents are provided in Tables 1–4.

Table 1 Illustrative quotes discussing family disclosure with the patient.
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Table 2 Illustrative quotes on aiding family disclosure.
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Table 3 Illustrative quotes on disclosure without patient consent.
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Table 4 Illustrative quotes on balancing rights and duties of family disclosure.
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Discussing family disclosure with the patient

There is a general consensus among the documents that HCPs have a responsibility to inform patients of the implications of results both for themselves and also for their family members (see Table 1).

Several documents additionally recommend that HCPs discuss the disclosure of genetic findings to at-risk family members with patients [12,13,14,15,16,17,18,19,20,21,22,23,24,25]. In the pretesting context, this may mean discussing the likely event that a patient would be encouraged to disclose information to their family members if a pathogenic variant is identified [12, 14, 16, 20,21,22,23,24,25,26,27]. Normative documents highlight the importance of these pretesting discussions about implications for, and disclosure to, family members for increasing the likelihood that a patient communicates the results to their family members following testing [20, 24, 27].

Many documents recommend HCPs advise patients to disclose information to relatives for whom it may be relevant after testing. Notably though, there is no clear consensus among the documents on the degree to which HCPs can (or should) be directive toward patients to disclose information to their family members. For example, while some documents imply communication of information to family members should be suggested [17,18,19, 28], others imply a much stronger approach is appropriate [22, 29]. Several documents go so far as to say that HCPs should try to persuade patients to inform their family members [12, 16, 24, 30, 31]. However, resorting to such measures may pose a concern for the autonomy of the patient. Despite this concern, the German Society of Human Genetics suggests it may, in some situations, be appropriate to attempt to persuade a patient to communicate genetic information to their family members [32].

Aiding family disclosure

Some of the documents indicate that health-care professionals may have further responsibilities to aid patients with disclosure beyond just informing patients of their need to disclose results to their family members. Several documents suggest HCPs should identify at-risk family members with whom it is important to share results (see Table 2) [13, 17, 18, 22, 24, 25, 27, 33].

Many documents support the provision of written information to patients such as family letters to facilitate the communication of genetic information [14, 22, 33]. Furthermore, several documents hold that HCPs should support patients and their families with counseling [14, 16, 24, 27, 33]. According to several documents, HCPs may be obliged to follow up, at least over the phone if not in person, to see if patients have communicated the results to relevant family members and provide counseling to further encourage and support disclosure if necessary [22, 33]. For families in which there is a problem hindering communication about genetic risk, additional counseling from psychologists and social workers is also recommended [14, 33].

Disclosure without patient consent

Some documents support the disclosure of genetic information to family members without patient consent as a last resort when the patient does not inform their family members. Due to the ethical complexity of cases of nondisclosure, it is often advised that HCPs discuss these cases with other health professionals or their institution’s ethics committee [21, 22, 24, 25, 29, 31, 34]. Such a case deliberation must determine whether the particulars of the case meet the conditions for disclosure without patient consent. The documents focus on assessing the clinical benefits for family members to reach a decision about the permissibility of disclosure without patient consent (see Table 3) [13, 24, 25]. Although most documents use “severity” to delineate between cases where disclosure without consent is and is not permissible, no guidelines define the concept of severity. Notably, there is no consensus among the guidelines regarding communication about untreatable conditions and the psychological impact that such information could have on family members. While a statement from the American Society of Human Genetics advises against disclosure in the case of untreatable or unpreventable conditions [13], the Australian National Health and Medical Research Council notes that while disclosure may not hold clinical benefit for the family members, it could have a positive impact on a family member’s psychology and management that could justify disclosure in some cases [24]. Furthermore, very few documents explicitly mention the relevance of genetic risk information for family members’ reproductive decision making as a condition for disclosure [12, 15]. If there is a possibility that disclosure without a patient’s consent could occur, documents recommend that the patient be informed of this [24, 25, 33, 35, 36].

Balancing rights and duties of family disclosure

The documents all acknowledge that the sensitive nature of genetic information warrants certain protections, including the patient’s right to confidentiality. As such, according to the guidelines it is generally not permissible for HCPs to share genetic information with anyone other than the patient unless the patient has explicitly consented to this disclosure [12,13,14,15,16,17, 19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44]. This right to confidentiality is acknowledged by almost all documents (see Table 4). On the other hand, most documents also acknowledge that the interests of the family should be considered. Most documents put the responsibility for the fulfillment of the duty to inform family members primarily on patients [12, 13, 20, 22, 24, 25, 27, 29, 30, 42]. In situations where patients fail to inform their family members, some normative documents hold that HCPs may also have a responsibility toward family members for whom the genetic information could have health or reproductive implications [12, 13, 15, 16, 19,20,21,22,23,24,25,26, 32,33,34, 36]. The documents differ in how they balance the patient’s right to confidentiality when it comes in conflict with the interests of family members for whom knowing their genetic risks could prevent serious harm. Notably, almost all documents support that there may be circumstances in which the family member’s rights may outweigh those of the patient [12, 13, 16, 20,21,22,23,24,25,26, 31, 33,34,35,36, 38, 39, 42]. However, while some guidelines mention that this situation may be possible, they resist directly supporting the HCPs right to inform family members without the patient’s consent and instead leave a degree of ambiguity about the permissibility of breaches in confidentiality in their guidance by stating that each case should be evaluated individually [32, 41]. French normative documents clearly prioritize patient confidentiality over the interests of family members [30]. Alternatively, some documents suggest that it may be possible to disclose genetic information while preserving the patient’s confidentiality. If a HCP decides to go forward with disclosure in the absence of patient consent, then it is required that they limit the information disclosed so as to reduce the chance of family members identifying the individual who underwent testing [20, 24, 25, 30, 33, 36].

DISCUSSION

This review provides a comprehensive analysis of normative documents that address family communication of genetic information. Our analysis identified that many of the documents provide recommendations for how HCPs can best facilitate family disclosure of genetic risk information, with several emphasizing the importance of early discussion of familial implications and communication with the patient. These recommendations are supported by empirical research in which HCPs cited cueing patients early to think about potential communication challenges as an important strategy for facilitating communication [45].

While some documents encouraged HCPs to help identify at-risk family members and provide patients with a letter to distribute to their families, they emphasized the patient, rather than the HCP, as the primary distributor of genetic information. There was less support in the documents for HCPs playing a more active role in family communication, despite evidence that patients support family communication by HCPs, particularly in cases where barriers to communication are present [46]. A review investigating how family communication of genetic information is addressed in genetic counseling found that cases of nondisclosure were likely to occur from patients having difficulty communicating the information, rather than their unwillingness to do so [47]. Therefore, normative documents could improve their clinical utility by providing more specific guidance on how HCPs can best support patients to communicate with their family members.

Notably, the only documents to state that patient confidentiality could under no circumstances be breached in the interests of family members were the French guidelines published in 1995 and 2003. However, in 2011 France enacted Public Health Code: L.1131–1–2 that legally binds patients to inform their relatives about genetic risks in the case of severe genetic conditions that are either treatable or preventable, including through genetic counseling. As such, despite the French normative documents in this review, the current French law requires that patients inform relatives either directly or indirectly with the assistance of the HCP who can distribute the family letter [48].

The severity and actionability of the genetic condition were cited by many of the documents as a reason for disclosure in cases where the patient is unwilling to inform their relatives. However, it was not always clear from the normative documents whether, and in which cases, the interests of family members could outweigh those of the patient. For instance, in the case of untreatable conditions, it was unclear from the documents whether disclosure to family members would be ethically permissible. This was particularly ambiguous for genetic conditions that are untreatable in the family member yet could be relevant for their reproductive decision making. An example of this has been demonstrated by the pivotal UK court case ABC v. St George’s NHS Trust, where HCPs failed to inform the daughter of their patient of her risk of Huntington disease that, while untreatable, had serious implications for her pregnancy [49]. The court ruled that HCPs have a duty to balance the interests of the patient and their relatives, and that in this case, due to the serious implications for the woman’s pregnancy, she should have been informed of her genetic risk despite the patient’s objection to disclosure. The narrow construction of clinical actionability that only considers the health benefits for the family members that was present in many of the normative documents may no longer be appropriate given the increasing accessibility and acceptability of reproductive technologies. In Australia, where national guidelines and legislation allow for disclosure of genetic information without the consent of the patient, a recent survey with HCPs found the lack of consideration of reproductive implications to be a leading concern regarding national guidelines and legislation [50]. Further research and deliberation are needed to more clearly define actionability as a reason for overriding patient wishes in cases of nondisclosure, particularly given that HCPs have reported difficulties with determining in which cases disclosure is permissible [9].

When mentioned, disclosure without patient consent is framed by the documents as a last resort to inform family members of their genetic risk. Almost all documents that discussed the possibility of disclosure without patient consent stated that each case must be deliberated individually. Despite this hesitancy within the documents to make definitive statements about the permissibility of disclosure in this context, there appear to be two main approaches taken with regard to who bears the ultimate responsibility toward family members. On one hand, French legislation places the duty to communicate on the patient who must do so either directly or request that their HCP do so on their behalf. If the family member realizes that they have not been informed of their genetic risk, it is primarily the patient who is accountable for this. On the other hand, the more common approach emphasizes the responsibility of the HCP to the patient’s family members, while still noting the duty of the patient. In documents that primarily emphasize the responsibility of the HCP, documents hold that the HCP is permitted to disclose in cases where the patient is unwilling to communicate genetic risk information. The recent UK court case ABC v. St. George’s takes the UK normative documents a step further from stating the HCP is permitted to disclose despite the patient’s objections to declaring that there may be cases in which the HCP has not only a professional or moral duty, but also a legal duty to inform family members [49]. Normative documents should consider and reflect the developments in the ongoing debate around the duties of HCPs to best guide HCP decision making and family communication.

Limitations

Our sample was limited by only including documents in English as well as the public Internet accessibility of normative documents. Further research on normative documents in other languages would provide a more complete understanding of norms of familial disclosure of genetic information without patient consent globally. Furthermore, our scope was limited to normative documents, and thus did not include legal documents that also could have relevance to the question of the permissibility of familial disclosure.

Conclusion

Normative documents should provide clearer guidance regarding the role of HCPs in supporting family communication of genetic information, particularly in instances where the patient has not consented to disclosure. The lack of clarity and discrepancies found between the normative documents in this analysis raise concerns regarding the ability of these documents to guide HCPs in decision making around the disclosure of genetic information to family members. In cases of nondisclosure, HCPs are faced with the conflict of how to balance their professional, ethical, and in some instances legal duties to patients and their family members, with research indicating that many HCPs lack the understanding and support necessary to make these decisions [8, 9, 50]. Organizations should try to provide clearer answers to questions around actionability as a criterion for disclosure without consent and what constitutes a fulfillment of a HCPs duties to family members. Providing clearer and more harmonized frameworks outlining in which circumstances family members should be informed and who should bear the responsibility of disclosing that information is necessary to facilitate the communication of genetic information to at-risk family members.