Introduction

Reproductive genetic carrier screening (RCGS) allows prospective parents to gain knowledge of their chance of having children with a serious autosomal-recessive or X-linked genetic condition. When a couple are both found to be carriers of a condition, they have an ‘increased chance’, of having an affected child [1]. As such, screening is offered preconception or in early pregnancy to facilitate greater reproductive choices [2]. Recent advances in technology have increased affordability of RGCS moving from single-gene testing e.g., Tay-Sachs disease [3] to allowing screening for multiple conditions (i.e., ‘expanded’ screening) driving international recognition of the benefits to population wide screening [4, 5]. In Australia, RGCS is predominantly available commercially to individuals or couples, however the cost and lack of public and medical practitioner awareness of screening exacerbates inequities of access and outcomes across populations [6, 7]. In response, and to reflect changing practice guidelines, some national health systems (e.g., Australia, Belgium) have started investigating population level RGCS [3].

Expanding the availability of RGCS requires non-genetic health care professionals e.g., general practitioners (GPs), obstetricians, fertility specialists and midwives to play an important role in offering RGCS. Decades of single-gene screening have provided a rich foundation of knowledge about health care professionals’ (HCPs’) perceptions towards offering population-based screening for individual conditions [8,9,10]. However, research examining expanded carrier screening has been limited primarily to genetic HCP or secondary HCP perspectives e.g., gynaecologists and obstetricians [11, 12] or focused on hypothetical offering in the primary healthcare setting [13, 14]. A recent review identified a predominance of practitioner level barriers (i.e., lack of practitioner confidence, interest) and organisational level enablers (i.e., professional bodies providing consistent advice) [15].

An in-depth understanding of this area is hampered by a lack of targeted implementation research examining the implementation of RGCS at a population scale. The introduction of new practices, such as offering RGCS, requires a change in practice of the HCPs. Behaviour change theory provides a way to analyse what is driving current behaviours (i.e., current practice) of HCPs and identify interventions that support the new desired behaviour [16]. Theory informed frameworks such as the ‘Capability, Opportunity, Motivation and Behaviour’ (COM-B) model and associated Theoretical Domains Framework (TDF) are effective for understanding contextual influences on desired behaviour [17]. The COM-B framework posits that behaviour is a result of our capability (C) (can we do the activity), opportunity (O) (is it possible to do it) and our motivation (do we want to do it) (M). The TDF consists of 14 domains and provides a more granular understanding of the influences on behaviour. For example, several TDF domains influence motivation (e.g., Emotion, and Belief about Consequences) and therefore align with the COM-B domain motivation (Fig. 1).

Fig. 1
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Alignment of Capability, Opportunity and Motivation, Behaviour (COM-B) and Theoretical Domains Framework (TDF) with abbreviations.

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In this study, we use qualitative methods informed by behaviour change frameworks, to investigate the experience of early adopters of RGCS in the context of a national research programme. Our objective is to gain an insight into HCPs’ perceived barriers and enablers to offering RGCS.

Materials and methods

Context

This study is part of a larger implementation science programme investigating strategies to support RGCS implementation in Mackenzie’s Mission. Mackenzie’s Mission is an Australian Government funded research study investigating how to optimally implement an easily accessible RGCS programme in Australia by offering couples free RGCS, testing over a thousand genes [18]. Details of the study are published elsewhere [18] but briefly couples were directed to the Mackenzie’s Mission website via an initial conversation with their GP, obstetrician, midwife, fertility specialist or genetics HCP. The portal contained information, a decision support tool and how to register. If the couple proceeded, they collected and posted in a cheek swab. HCPs were not included in this process but were informed of results.

Research design

We employed a qualitative approach using semi-structured interviews with a subset of participating HCPs to gain a rich understanding of the meanings and interpretations behind individuals’ behaviour towards offering RGCS through Mackenzie’s Mission [19]. We adopted descriptive phenomenology which can be used to study an area of interest from the perspective of those involved [20], using behaviour change theory as our methodological framework.

Participants and recruitment

Throughout the study duration, HCPs from various settings in all Australian states and territories (including general practices, private/public obstetrics and midwifery practices, fertility clinics, and community health services) were able to self-refer into the Mackenzie’s Mission study or were invited by study genetic counsellors. As the focus of the study was on preconception RGCS, the intention was for most couples to be recruited via GPs. HCPs who agreed to be part of Mackenzie’s Mission were provided with an education session about RGCS and the study processes before being able to offer Mackenzie’s Mission RGCS to their patients.

HCPs who expressed interest via a pre-education questionnaire and had been offering Mackenzie’s Mission for >8weeks were contacted via email, by the implementation research team, and invited to take part in either a telephone or videoconference interview. One follow-up invitation was sent for those who did not respond to the initial contact. Using purposive sampling [21], we selected over 150 eligible HCPs (n = 168) to invite to take part in an interview. HCPs were from a range of professions and levels of experience of RGCS, in particular GPs as the predominant referrers, and different state/territories. Those HCPs who declined to participate in the Mackenzie’s Mission study were also offered an opportunity to interview.

Data collection tools and procedures

An interview guide (Supplementary File 1) was developed using the behavioural framework COM-B, as a way to categorise sources of behaviour [22]. For example, ‘what experience do you have with RGCS?’ (C); ‘Starting off, was there anything that would have made offering RGCS easier?’ (O); and ‘What made you decide to offer RGCS?’ (M). Participants were asked about their experiences of offering RGCS and their views on future RGCS service planning. Whilst the structure of the guide remained the same, constant iterative comparison [23] of the interview transcripts led to minor revisions in the interview schedule. Interviews were designed to take around 30 min, and scheduled at a time convenient for the HCP. Interviews were disrupted by the SARS-CoV-2 pandemic and began in August 2020, finishing in August 2021 when data saturation and maximum variation in sample was reached. Interviews were conducted by three qualitative researchers (SB, JL and ZF) who had no prior relationship with participants. All interviews were audio-recorded, de-identified and transcribed verbatim. Audio-recorded verbal consent was sought and recorded before the interview.

Data analysis

Interview data was managed in NVivo 12 [24]. Analysis was guided by the TDF. A coding guide that incorporated the TDF was adapted to the specific context (Supplementary File 2), revised from a previously published guide [25]. An important first step to using the TDF is to define the target behaviour i.e., the core activity that is essential for a change in practice to occur. For this study ‘offering RGCS’ was identified. However, during analysis, two additional target behaviours became evident. 1. Engaging with RGCS—how HCPs initially start thinking about offering RGCS; 2. Identifying eligible patients to offer RGCS to—including pre-conception; and finally the original target behaviour, 3. Offering RGCS to patients—incorporates the discussion with potential patients their perceived receptivity and following required process. Transcripts were examined and deductively coded using the coding guide (Supplementary File 2) to identify factors that facilitate or hinder HCPs when offering RGCS. Initially, five transcripts were coded independently by two researchers (SB and ZF) and compared for discrepancies. One researcher (ZF) completed the coding with ongoing regular meetings (SB and JL) to discuss and resolve challenging coding and findings. Reflecting the complexity of offering RGCS, overarching barriers were identified first before detailing the underlying barriers and determiningtheir associated TDF coding (SB, ZF and JL).

Results

Participant characteristics are presented first, followed by the analysis of the three target behaviour barriers and enablers and associated TDF codes.

Characteristics of participants

Overall, ~1000 HCPs were enroled in the Mackenzie’s Mission study. Of the 168 eligible HCPs invited to an interview, thirty-one agreed. The few participants who actively declined and gave reasons noted they were too busy especially because of the SARS-CoV-2 pandemic or they had not offered RGCS due to seeing different patient cohorts. No HCP who declined to participate in Mackenzie’s Mission indicated they were available for a follow-up interview. On average interviews ran for 24 min most were undertaken via videoconference and one participant opted for a telephone interview. Table 1 summarises the characteristics of interview participants who were predominantly GPs (74%) working in metropolitan areas of Australia (84%) with a fair proportional distribution amongst states per population size. Most participants had prior experience of offering RGCS (68%) and eight (26%) had experienced a patient receive an increased chance result as part of the Mackenzie’s Mission study.

Table 1 Sample characteristics.
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Barriers and enabling factors by target behaviour

From the interviews, 15 barriers and 44 enablers (6 of which related to specific programme components of Mackenzie’s Mission) were identified across the three target behaviours 1. Engaging with RGCS, 2. Identifying eligible patients to offer RGCS to, and 3. Offering RGCS to patients. Whilst all TDF domains were present, barriers were predominantly categorised as ‘Environmental Context and Resources’ followed by ‘Knowledge’ and ‘Beliefs about Capabilities’ (Fig. 2). Here, we outline the barriers and report recurrent enablers as reported by participants, further details are reported in Tables 2–4.

Fig. 2: Overview of target behaviours, barriers and enablers to offering reproductive genetic carrier screening.
figure 2

Abbreviations: (Kn) Knowledge, (ECR) Environmental Context and Resources, (SPRI) Social Professional Role and Identity, (BCon) Beliefs about Consequences, (MAD) Memory, Attention and Decision Making, (SI) Social Influences, (Sk) Skills (Breg) Behaviour Regulation, (Rein) Reinforcement, (Em) Emotion, (Opt) Optimism, (In) Intentions.

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Table 2 Detailed summary Target behaviour 1: Engaging with RGCS.
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Table 3 Detailed summary of Target behaviour 2: Identifying eligible patients.
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Table 4 Detailed summary of Target behaviour 3: Offering RGCS to patients.
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Target behaviour 1: Engaging with RGCS

Two overarching barriers were identified: awareness, understanding and education about RGCS and HCPs’ attitudes towards and beliefs about RGCS. Figure 2 and Table 2.

Awareness and understanding of RGCS: Three barriers were associated with a lack of, or low knowledge of, RGCS within primary health care.

  1. i.

    Low awareness of RGCS (TDF: Knowledge) especially compared with other antenatal tests (e.g., [NIPS]). Enablers included promotion by their peers, professional bodies, and their patients raising RGCS (TDF: Social Influence).

  2. ii.

    Low understanding (TDF: Knowledge) of RGCS was reported by many HCPs. Education sessions that allowed HCPs to ask questions were cited as a helpful way to improve understanding. (TDF: Knowledge and Social Influences).

  3. iii.

    Time/logistics of participating in education (TDF: Environmental Context and Resources), was found to be time consuming, taking away from direct patient contact, though enabled by receiving professional development points (TDF: Reinforcement) or making education available through different modes (TDF: Environmental Context & Resources).

HCP attitudes towards and beliefs of RGCS (TDF: Social and Professional Role and Identity): Two barriers were identified in this overarching barrier.

  1. i.

    Lack of HCP interest (TDF: Social and Professional Identity), for some HCPs this is attributed to not seeing the relevant population of patients though others did not feel offering screening was part of their role. Enablers include inter-practice referrals (TDF: Environmental Context and Resources).

  2. ii.

    Concerns about negative effects (TDF: Belief about Consequences) e.g., patient anxiety about screening or financial implications for families who receive an increased chance result. However, emotional connection acted as an enabler (TDF: Emotion).

Target behaviour 2: Identifying eligible patients

One overarching barrier was identified in this target behaviour, opportunities to identify eligible patients. Figure 2 and Table 3.

Opportunities to identify eligible patients

Three barriers were apparent within this overarching barrier: environmental factors (TDF: Environmental Context and Resources); forgetting to offer (TDF: Memory Attention and Decision Making); and patients’ personal situations (TDF: Belief about Consequences).

  1. i.

    Environmental factors (TDF: Environmental Context and Resources). One HCP reported they would be unlikely to see a patient (especially a female patient) in a reproductive healthcare context, a sentiment shared by some of the female GPs when speaking about their male colleagues. Others were concerned about when to time making the offer and questioned whether early pregnancy was an appropriate time. Several participants reported initiatives to raise awareness of RGCS could function as an enabler (TDF: Memory Attention and Decision Making) to prompt a change in patients initiating the conversation with their HCP.

  2. ii.

    Forgetting to offer (TDF: Memory Attention and Decision Making). Missed opportunities to identify patients were commonly cited, especially HCPs forgetting RGCS due to competing priorities. Most participants spoke about making RGCS a priority in their practice, so that offering RGCS becomes part of routine practice, including for same sex couples (TDF: Intentions). Some incorporated offering into other screening visits (TDF: Behavioural Regulation) such as cervical screening.

  3. iii.

    Perceptions of patients’ personal situations (TDF: Belief about Consequences). Some HCPs were mindful about raising anxiety for women they see in early pregnancy assessment clinics or ensuring they take patient’s cultural beliefs into consideration. Some reflected on their messaging to be clear that preparing if a child may require early intervention or have special needs can be helpful. Being able to build rapport with patients through continuity of care allowed HCPs (especially midwives) to judge each situation on a case-by-case basis (TDF: Skills) and ensure RGCS was offered, or even just mentioned as an option to patients regardless of their situation.

Target behaviour 3: Offering RGCS to patients

Two overarching barriers were identified in this target behaviour, providing pre- and post- test counselling, and patient receptivity. Figure 2 and Table 4.

Providing pre- and post- test counselling

HCPs reported four interrelated barriers to counselling during these phases.

  1. i.

    Low consumer awareness (TDF: Environmental Context and Resources). HCPs reported low consumer awareness of RGCS and patient confusion with other prenatal tests (i.e., NIPS). Consequentially, HCPs described a sense of responsibility to take the time to increase awareness and explain in an easily digestible way what RGCS involves and considered themselves well placed to at least raise the topic (TDF: Social and Professional Identity).

  2. ii.

    Concern about ability to counsel (TDF: Belief about Capabilities) were reported by some HCPs especially when not regularly providing pre- and early pregnancy care including, mixing up RGCS and NIPS or raising potentially worrying or distressing information. Genetic counsellors were favoured as a resource for HCPs to seek guidance, others sought peer advice (TDF: Social Influences), and some felt practice was key (TDF: Skills). Particularly for post-test counselling, HCPs reported they valued having access to genetic counselling support as needed for both themselves and for couples (TDF: Environmental Context and Resources and Professional Role and Identify). HCPs who had patients take up testing felt more confident in their abilities and in some cases felt rewarded, experiencing patient gratitude to be offered RGCS.

  3. iii.

    Time constraints (TDF: Environmental Context and Resources) were a dominant challenge. Coupled with the previous barriers HCPs were concerned about the time to inform patients about RGCS. HCPs found the Mackenzie’s Mission website helpful in this situation, when there were time constraints they would provide the website and encourage patients to review the content in their own time (TDF: Environmental Context and Resources).

  4. iv.

    Regional barriers (TDF: Environmental context and resources). HCPs consider the Mackenzie’s Mission model facilitated couples living in regional and remote areas acceptable access and was successfully offered via telehealth. Outreach services providing education and offering RGCS was cited as a model that could be used in addition, to reach communities with limited access to healthcare (TDF: Environmental context and resources).

Perceptions of patient receptivity

HCPs perceived three barriers in relation to patients’ receptivity to RGCS.

  1. i.

    Financial barriers (TDF: Environmental Context and Resources). Cost was identified as a previous barrier to offering testing, and looking to the future, HCPs felt funding should cover GCs counselling for increased chance couples (TDF: Environmental Context and Resources), whereas the additional services included in Mackenzie’s Mission (e.g., one round of IVF) whilst generous were considered unlikely to be sustainable.

  2. ii.

    Patients’ religious and ethical beliefs (TDF: Intentions). Patients’ religious beliefs, or patients with ethical concerns around termination of pregnancy were discussed by some HCPs. In most circumstances, HCPs felt they could still provide patients with the information that allowed them to make an informed choice in line with their values, framing the conversation around the benefits of knowing your carrier status (awareness and preparedness, becoming knowledgeable about the condition, talking to specialists, joining support groups etc.) (TDF: Skills).

  3. iii.

    Not knowing whether the sample has been supplied (TDF: Environmental Context and Resources). Some HCPs ant to be made aware when a couple provided a sample to the laboratory for screening to accommodate follow-up appointments. Here, HCPs could follow-up with the patient if required (TDF: Reinforcement).

Discussion

To support any change in a behaviour or activity, such as offering RGCS, it is essential to clearly specify the target behaviour(s) required and the associated barriers and enablers at each stage. Without this understanding there is a risk of investing resources to design solutions for potentially non-existent problems, wasting time and effort [26]. This study investigated the experiences of HCPs, with particular focus on non-genetic professions, offering population RGCS and categorised findings into three sequential target behaviours: 1. Engaging with RGCS, 2. Identifying eligible patients to offer RGCS to, and 3. Offering RGCS to patients. We identified 15 associated barriers and significantly more enablers (n = 44) which could reflect the nature of the participants, who as early adopters are often positive about the change and are understood to influence the behaviour of those around them by making the behaviour change more observable [27]. Indeed, social influences were shown in this study to be a principal factor in HCPs’ initial engagement with RGCS and increasing awareness amongst their peers and will play a key role in the success in the roll out of future population RGCS programmes. Acknowledging previous research undertaken in this area, here we discuss HCPs’ preferred option for offering RGCS through a comprehensive model of care, like the approach taken in Mackenzie’s Mission, the associated challenges and identify implications for future service delivery. TDF domains are indicated with bold text.

The Mackenzie’s Mission model of care required HCPs to provide the offer of testing and direct the couple to a study participant portal. There the couple were provided with education and a decision aid to make informed decision about RGCS. Although this approach was designed to minimise the time taken for HCPs to offer RGCS, it meant HCPs lacked knowledge of the patients’ journey and did not know whether the patient had in fact accepted the offer of screening. Understanding their role in the process appeared key to HCPs improving belief about their capabilities in incorporating this more ‘hands off’ way to offering RGCS into their practice. Some HCPs hoped the model, especially the online education and consent which is favoured for overcoming the complexities of consent in genomic medicine [28], would continue when RGCS becomes more widely accessible.

Equity was raised by many participants. We did not capture data on HCP ethnicity which may have provided a useful lens with which to analyse some HCP comments and assumptions on when to offer RGCS or not. Some HCPs expressed concern about when it would be appropriate to offer screening for some communities e.g. migrant populations. There is the risk of unconscious bias acting as a barrier to equity of access through the offer, or lack of to RGCS. Whilst no access to technology barriers were reported, several HCPs raised concerns about potential consequences due to language barriers for couples from culturally and linguistically diverse backgrounds being able to access online material without HCP assistance [29]. The availability of online translation services may help overcome these concerns [30]. Overall, the ease of access was found complimentary to telehealth and an acceptable way to offer RGCS for regional/remote areas. The model also worked for donor couples, where the donor could provide a sample, allowing HCPs to be able to offer equitable care.

Accessing RGCS through Mackenzie’s Mission still requires HCPs to have the knowledge and skill to identify patients for whom RGCS is appropriate. Within the Mackenzie’ Mission programme an extensive amount of work has been conducted and reported on the role (and design) of education in the implementation of genomics and large-scale carrier screening programmes. Despite widespread consensus that RGCS is best situated in primary care, aligning with HCPs’ professional identity, and offered pre-conception [2, 7, 31], research shows higher uptake among pregnant women [32]. Not only does offering pre-conception allow couples access to greater reproductive options, but our study also indicates offering in pre-conception lessens other HCPs barriers (e.g., environmental time constraints in antenatal appointments, and HCPs concern about the potential consequences for patient anxiety). However incorporating the offer of RGCS into pre-conception care (public funding capped at 40 min) appeared to be more challenging, due to a lack of resources and forgetting to offer due to competing priorities in short appointment sessions with HCPs finding it easier to discuss RGCS when the conversation is initiated by the patient [9]. This lack of time will remain a key challenge and identifying mechanisms to support HCPs will be essential to drive successful take up and implementation of future RGCS programmes. Undoubtedly, raising community awareness of RGCS as a part of pre-conception care is needed to facilitate greater patient receptivity and ability to make informed decisions about screening. As patient health literacy was considered an enabler for HCPs to offering RGCS, increasing consumer awareness may also improve equity of access. HCP skill and intentions to incorporate RGCS into general practice appointments was an attributable factor to opportunistically identifying pre-conception patients. Although HCPs found raising RGCS in early pregnancy easier, some HCPs expressed concern about the consequences with the potential of upsetting the couple during this period. Fears of medicalising pregnancy have previously been identified [13, 33] and additional tools (e.g., decision aids [34]) are required to ensure couples can make decisions that align with their values [32].

Unlike the other target behaviours, HCPs did not recognise any Mackenzie’s Mission specific supports provided for the second target behaviour, identifying eligible patients. Where enablers are lacking, often in more complex areas (e.g., forgetting to offer RGCS pre-conception—TDF Memory Attention and Decision Making) the application of the behaviour change theory, through coding with the TDF [35], can offer additional theory informed behaviour change techniques using the Theory and Techniques Tool [https://theoryandtechniquetool.humanbehaviourchange.org/] [36] to support HCPs. For example, theory informed behaviour change techniques aligned with Memory, Attention and Decision Making include ‘prompts and cues’, e.g.,, setting a reminder on the GP information system to prompt the ‘One Key Question®’ [37] discussion with all patients of reproductive age to ask if they are planning a pregnancy in the near future. If yes, the HCP can share a range of health considerations including the option of RGCS.

One reported area of concern was the need for counselling couples who receive a 1 in 4 chance of affected children with HCPs’ belief about their capabilities. The Mackenzie’s Mission model ensured a study genetic counsellor was available and they played a critical role in supporting HCPs with expert knowledge and skills, and also couples, as they made reproductive decisions to align with their values. Further provision of RGCS through primary care will require careful consideration of how genetic counselling services could be provided [34, 38, 39]. Given HCPs perception of their own ability of offer RGCS appears to be contingent on availability of expert genetic counselling and clinical support, it is essential that population-based programmes provide this support.

In addition to HCP individual level experiences noted here, future implementation of national RGCS programmes while dependent on local context [40] may benefit from aspects of programme design. Figure 3 reports several features identified from this study that can contribute to making reproductive genetic carrier screening more accessible.

Fig. 3
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Examples of aspects of programme design that can contribute to reproductive genetic carrier screening being more accessible.

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Limitations

Drawing on the experience of early adopters is likely to have introduced positivity bias, with the possibility that HCPs who were likely to respond to interview invitations were those most likely highly engaged with Mackenzie’s Mission. Mitigating that, a third of participants had no previous experience with RGCS. Of the 168 potential participants we only interviewed 31 either due to lack of response or the HCP was unable to participate. We were also unable to capture the views of those who declined to participate in the Mackenzie’s Mission study. The SARS-CoV-2 pandemic led to data collection taking over a year, which was longer than planned, meaning some external contextual factors may have changed. This study was undertaken in the context of an Australian Government funded research project where generalisation may be limited to Australian health system and a well-resourced research project (under Mackenzie’s MIssion, RGCS is offered free of charge to the couples, genetic counselling is offered to couples receiving a high-chance result and to support HCPs so may not reflect other health systems or state-wide or national RGCS programmes.

At present, RGCS is offered in an ad hoc manner and access is variable. Whilst population-based approaches will make access more equitable, targeted support for HCPs to offer patients the option of RGCS is required. Behaviour change theory provides a structured approach to learning from the experience of early adopters and an opportunity to identify the determinants influencing implementation. The key steps of collection and coding of barriers and enablers by each target behaviour identified outlined here can now be used to select and test theory informed implementation strategies. Although this study shows HCPs’ strong preference for offering RGCS through a comprehensive model of care, and various other programme design elements that reduce barriers, it is essential that future research continues to leverage behaviour change theory to develop and test programme design elements that contribute to RGCS being provided in an equitable and accessible way.