Stage 1: Identifying the research question/objective

An overarching research question guided our systematic search strategy and reporting of results:

What is known from the existing literature about parents’/caregivers’ fears and concerns regarding their child’s epilepsy, their perceptions of the impact of their fears and concerns on family life, and on their own social and emotional well-being and what mitigates these fears and concerns? This question enabled us to adequately capture a broad range of existing literature while providing the opportunity for further research objectives to be added and modified throughout the review. This iterative process was useful as we became increasingly familiar with the literature although we did not need to amend the objectives.

Stage 2: Identifying relevant studies

Our definition of fears and concerns was broad and encompassed anything reported as a fear or concern within the papers; this included terms such as worry, anxiety, psychological distress, and hypervigilance.

Search terms were developed based on consideration of the population (parents/caregivers of children aged ≤ 18 years with epilepsy, families); concept (parents’/caregivers’ fears, concerns, anxiety about their child’s epilepsy); and context (any setting) [28] (S2 Table). Keywords and terms were identified by the authors, other members of the CASTLE (Changing Agendas on Sleep, Treatment and Learning in Childhood Epilepsy) research study team and parents from the study’s Family Advisory Group (castlestudy.org.uk).

A comprehensive list of search terms was identified and refined through searches on Scopus and Medline by the review team. AR and GC led the development of the search strategy with the support of a health research librarian. Truncation and proximity operators were employed to increase the sensitivity of the search (S3 Table). Searches were undertaken in Scopus, Medline, CINAHL and PsychInfo databases in March 2021 (S4 Table).

The reference lists of included papers were reviewed for additional papers, and Scopus and Google Scholar were consulted to identify the citing literature. A search of the grey literature (reports and webpages), including a hand search, was also completed in March 2021 (S4 Table). Grey literature was identified using similar search terms to those used in the main search via Open Grey, Google Scholar and from the websites of NICE Evidence search, Royal College of Paediatrics and Child Health, Royal College of Nursing, National Institute of Health Research portfolio, Department of Health, Epilepsy Action, Epilepsy Society, Epilepsy Research UK, Young Epilepsy, Epilepsy 12, International Bureau for Epilepsy (IBE), International League Against Epilepsy (ILAE), as well as other international epilepsy organisations. The Google Scholar search produced 7150 results, the first 520 were hand searched; this was a reasonable number of references to consider as recommendations are that for systematic review searches focus on the first 200–300 results [29].

Stage 3: Study selection

Studies were included in the review if they met the criteria outlined in Table 1. The original search parameters were papers published 1st January 2010 – 23rd March 2021; it was updated on 15^th April 2022. The year range was limited to studies published from 2010 onwards as the focus was to explore relatively recent literature so that any recommendations for practice would be contemporary and meaningful. The parents/caregivers of children aged ≤ 18 years was used to encompass children and young people and was determined based partly on the World Health Organization (2014) [30] definition of a ‘child’ as a person under the age of 18 years but also reflecting that many studies of children include 18 year olds and we did not want to miss such studies from the review.

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Table 1. Inclusion and exclusion criteria.

https://doi.org/10.1371/journal.pone.0274001.t001

Inclusion criteria and types of sources

The inclusion and exclusion criteria are shown in Table 1.

In Stage 1 papers (n = 8714) were imported into Covidence (systematic review software) for screening, duplicates (n = 4637) were removed. Titles and abstracts of all papers (n = 4077) were blind reviewed by at least two members of the review team (AR, GC, BC, AC and LB) and conflicts resolved by a third reviewer from the team. One paper was unavailable in full-text format and was excluded [31]. In Stage 2, members of the review team (AR, GC and BC), were allocated papers with two reviewers each screening all full-text papers (n = 110). Twenty-four papers met the inclusion criteria and aim of the review. Conflicts were resolved through discussion between the two reviewers or where further advice needed by a third reviewer (see Fig 1).

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Fig 1. PRISMA flow chart of the scoping review search.

https://doi.org/10.1371/journal.pone.0274001.g001

Stage 4: Charting the data

We developed a data extraction sheet which we iteratively refined and included the following broad categories: fears and concerns, impact of fears and concerns, similarities/differences between children and parents/caregivers, and mothers and fathers, mitigations and risk factors. In line with the aims of a scoping review, all fears and concerns were included in the data extraction sheet (see S5 Table). Reviewers (BC, GC, AR, LB) independently extracted data from their allocated articles with extractions checked for consistency and condensed by one reviewer (BC).

Stage 5: Collating, summarising, and reporting results

Information from the included papers was collated and summarised within the data extraction table (S5 Table) and this proved invaluable in helping to develop initial themes which were refined and finalised through discussions involving all members of the research team.

Stage 6: Consultation

A key stage of Arksey and O’Malley’s [23] framework which is often not used within scoping reviews, is the sharing of review findings and consultation with members of the associated audience. We were determined to ensure our review modelled good practice and core to our review was engagement with parents in the Family Advisory Group who have experience of their children’s epilepsy at key stages during the review. This involved us asking for their input during one of their regular meetings about the scope of the review question, identification of search terms and key words and review of findings. So, for example, they were interested in our review encompassing both existing as well as future fears and concerns and we added this element to the review question. In reviewing our findings parents provided feedback on how the reviewed research resonated with their own thoughts and experiences.

Overview of included studies

In total, 24 papers were included in the review and each paper was treated as a separate study; however, three papers by Webster [32–34] may be part of one study and two papers by Benson [35,36] may be part of one study.

Data are reported on studies undertaken in the USA (n = 4) [37–40], Ireland (n = 3) [35,36,41], Canada (n = 3) [42–44], UK (n = 4) [32–34,45] and one each in Australia [46], Brazil [47], Greece [48], India [49], Iran [50], Malaysia [51], Mali [52], Serbia [53], Sri Lanka [54], and Zimbabwe [55].

Parents’/caregivers’ fears and concerns regarding their child’s epilepsy

Impact of epilepsy-related fears and concerns on the daily lives of children and parents/caregivers

Impact of epilepsy-related fears and concerns on parents’/caregivers’ social and emotional well-being

Emotional impact of parental fears and concerns. Five studies reported on the emotional impact of their child’s epilepsy with parents’/caregivers’ experiencing worry, shock, upset and anxiety [35,43,44,46,51]. Parents/caregivers feared the distressing aspects of witnessing the physical manifestations of seizures [35].

There were specific time points when or areas of concern where emotional reactions were experienced. This included shock, worry and upset during the child’s first seizure [51], devastation, confusion, and worry at the point of diagnosis [35,44], anxiety around the risk of SUDEP, which reduced when the low risk of SUDEP was explained [43], as well as feeling vulnerable and helpless if they could not control their child’s seizures [46]. Parents/caregivers also felt anxious and stressed about explaining their child’s condition to their child’s school community resulting in lacking a sense of belonging with the school [44], anger and sadness in response to the offensive reactions of others [35] and experienced negative emotions often motivated by negative stereotypes of epilepsy [47]. In one study, mothers blamed themselves or some were blamed by their in-laws for ‘causing’ the child’s epilepsy [51] and emotional impact was evident in one study where epilepsy was believed to be caused by bad spirits [51]. Parents/caregivers reported the impact of epilepsy related fears and anxiety on their sleep because of the need for increased vigilance [47] resulting in them feeling exhausted [38].

In one study where mothers and fathers’ emotional experiences at the point of diagnosis were investigated showed that mothers often experienced mental health issues while fathers experienced feelings of worry and anger (at healthcare team) as well as concern for their family [43]. Fathers also reported feeing uncertain and frustrated at the lack of practical approaches to managing SUDEP [43]. In another study, fathers feared the impact of their child’s condition on their own identity such as being viewed the father of a handicapped child [48].

Study limitations

It is important to recognise the limitations reported by the authors of the reviewed studies. Commonly authors recognised sampling bias including non-probability sampling [55], self-selection bias [35]; 10 studies (encompassing both qualitative and quantitative methods) indicated that their samples may not be representative [38,41,43,45,47,49,51–53,55]. Furthermore, six studies recognised the limitations of small sample sizes which may not be representative all parents/caregivers of children and adolescents with epilepsy [39,40,42,47,49,54]. Five studies acknowledged bias due to the over-representation of mothers or female caregivers [35,36,40,45,46]. Nine studies acknowledged limitations relating to the child’s diagnosis of epilepsy, for example, recruitment was limited to specific types of epilepsy [35,41], where children had co-morbidities [46,54] had seizures that were well-controlled [39,48,51], had severe epilepsy [40] or unknown seizure type [55]. Finally, authors acknowledged limitations regarding the methods employed, including interview methods [45] or lack of validation of survey methods [49].

Study recommendations for practice

Overall, five studies recommended good quality tailored communication between healthcare professionals and parents/caregivers [36,37,41,47,48]; although the evidence-base was variable. Five studies recommended that (some) parents/caregivers would benefit from some form of tailored psychological support at various stages of the trajectory (diagnosis onwards) (e.g., counselling) to help them manage some of the fears (stigma, SUDEP) and challenges (e.g., disclosure) they faced [36,43,46,48,50]. One study recommended that interventions should be developed to support parents/caregivers and/or promote resilience [40] and three specifically suggested that parents/caregivers could benefit from signposting to [37] or engagement with other parents/caregivers of children with epilepsy and with epilepsy-focused support groups [46,48]. Raising the awareness of healthcare professionals about the impact of epilepsy on the psychosocial health of parents/caregivers was recommended in one study [55]. Two studies identified the need for the development of good education resources to promote informed parents/caregivers and children [41,48]. Five studies recommended greater efforts should be made in terms of advocacy and improving public (e.g., schools, community) awareness and information about epilepsy as this could reduce issues such as stigma [36,49,50,52,53]. Three studies recommended that account should be taken of cultural sensitivities related to epilepsy [49,52,55]. Nine studies did not report recommendations [32–34,38,39,42,44,45,51].

Study recommendations for future research

A variety of future research studies were proposed; these could be broadly categorised as child/parent focused, communication focused, and impact focused. Two studies proposed work addressing the resonance or differences in the perspectives of parents/caregivers and children in terms of concerns and/or knowledge [33,54]. Future communication-related research included work addressing better communication between parents/caregivers and healthcare professionals [45], supporting parents’ communication with their children [32], and considering a range of issues related to disclosure [32,35]. Two studies proposed future research should address impact; one wanted to develop a tool for assessing caregiver impact [38] and the other proposed to explore the best way of supporting parents/caregivers to navigate systems and access resources [45]. Eleven studies did not report any plans for future research [34,36,37,39,40,46,48,50–53].

Fears and concerns create a sense of threat

In the current review, it was clear that parents/caregivers experienced a wide range of threats in the form of fears, concerns and worries. The threat from these fears and concerns triggered a legitimate need to protect their child, but as noted in the CFT model [57,58] an over-active sense of threat can generate a negative emotional response. The findings show there was a pervasive fear associated with the unexpected and uncertain nature of parenting a child with epilepsy [34,38,40,44,51]. The review findings align with previous research that suggests that the challenge of managing the day-to-day care of their child can be exacerbated by the often unpredictable nature of their child’s condition [67].

The review findings reveal that the day-to-day reality of living with these fears resulted in increased vigilance [47], sleep deprivation [38] and negative emotional wellbeing, all of which may function to exacerbate parental fears, stress or result in overly restrictive or perceived protective behaviours [33,40,43,46,47,51]. Evidence from studies in the current review concur with previous research that parents of children with epilepsy and other long-term conditions experience increased negative emotional outcomes such as parenting stress [12,19,21,55,68] and perceived overprotective behaviours [69].

Evidence from studies in the current review suggest some of the parents’/caregivers’ fears reflected concurrent threats to their child’s existing circumstances such as their child’s seizures, the impact of these on the child and the impact of anti-seizure medication. Broader threats related to the societal implications such as social stigma [35–37,40,44,47,48,51,54,55] and/or disclosing [35,36,44,49–51] their child’s condition, as also seen in studies of children with long-term conditions [70–72]. However, other fears were more future-focused, for example pervasive fears about their child’s future health [37,38,51], opportunities and abilities [34,40,51,54,55]. These fears appear to reflect empirical evidence that children with epilepsy can have reduced medical, psychological, social and cognitive outcomes [73–75].

A key distinction emerged from studies in the current review between the threats, fears and concerns that parents had some control over (e.g., adopting protective behaviours such as limiting travel away from home, restricting child’s activity participation [44,49,50,54,55]) and ones where they had much less control (e.g., the child’s seizures [35,38,42,43,46,50,54] and the social implications of their child’s condition, such as bullying [36] and/or being treated differently [35,36,44,48,51,54]). Epilepsy-related fears about factors outside of parents/caregivers control commonly negatively impacted parents’/caregivers’ emotional and social well-being, as also seen in other studies of parents/caregivers of children with long-term conditions [19–21,76,77].

The drive to protect their child from threat

As seen in the review findings, parents/caregivers were clearly motivated (driven) to protect their child from the various threats that they perceived, and whilst ‘drive’ can be positive an over-active sense of drive can generate a negative emotional response [57]. Evidence from the review highlights that parents/caregivers felt they lacked appropriate knowledge or information about their child’s condition [34] as well as awareness of where to source information about their child’s condition [41]. Potentially, better access to information and resources could positively influence both the threat and drive systems; certainly recommendations from the reviewed studies propose that parents would benefit from tailored information [36,37,41,47,48], professional support [36,40,46,48,50] and peer support [37,46,48]. For example, the current review findings highlight that perceived threats from disclosure resulting in selective disclosure, which echoes concerns held by children with epilepsy reported in previous work [6].

The need for information and support; the search for security and regulation

As discussed above parents’/caregivers’ fears and concerns created a threat and a drive to try and protect their child. However, the findings of the review indicate that many of these fears continued to dominate their lives as little acknowledgments and/or support was available to mitigate these concerns. In the CFT model, the ‘soothe’ system aims to help regulate the threat and drive systems and when this does not happen people feel unsafe and insecure [57]. Parents/caregivers desired information, advice and support [33,41,45] in their search for a greater sense of security about their child’s seizures and those aspects of their child’s epilepsy that were ‘more than just seizures’. Where explanations are provided, for example about the low risk of SUDEP, anxiety can be reduced about this fear [43]. The recommendations of the studies in this review highlighted the current lack of and the need to offer psychological support to parents/caregivers to help them manage fears and the impact of these fears (threat).

The fears and concerns perceived by parents/caregivers identified in the current review represented a broad and significant threat. What is not clear from the review is to what extent the ‘threat agenda’ of parental/caregiving fears aligns with the often more seizure-focused ‘clinical agenda’ of clinicians and how this may impact meaningful dialogue within clinical consultations. The review findings align with other work that suggest that parents/caregivers and clinicians can have different perceptions about child seizures and their impact [78] and both the level and sources of threat. Such different, albeit overlapping, agendas can result in parents/caregivers not receiving answers to questions they may find difficult to frame and clinicians missing opportunities to provide information about issues they do not appreciate are of concern to parents/caregivers. As seen in other studies, clinicians may offer reassurance to parents that does not meet their needs and lacks meaning [79]. The review highlighted that many parents/caregivers may benefit from psychological support to help them manage fears and the impact of these fears (threat).

The review findings suggest that a collaborative ‘agenda’ for thinking about childhood epilepsy is necessary and could help frame clinical consultations in a way that could address the medical concerns of clinicians as well as mitigate the wider emotional, psychosocial and societal concerns of the parents/caregivers. Such an agenda could be developed between children with epilepsy, their parents/caregivers and clinicians and could build on existing work such as the core outcome set (COS) for childhood epilepsy [17] developed at an earlier stage of the CASTLE programme [66].

In the UK and elsewhere some, but not all children and parents/caregivers, will have access to an Epilepsy Specialist Nurse (ESN) whose remit is to provide parents with information, advice and support about their child’s medical condition but also on coping with the wider challenges [80]. Consistent support for all parents of children with epilepsy from an ESN and acknowledgments of their fears and concerns could be an important way of validating and mitigating the threat reported by parents/caregivers in the review. The potential for peer-to-peer parent support was suggested in the review [46,48] and has been shown to be beneficial in other studies of parents/caregivers caring for children with long-term conditions [81]. Benefit may result from structured group-based intervention to support the health and well-being of parents/caregivers, as already established for parents/caregivers of disabled children [82,83].

The discussion of the findings of the review within the three affect systems of the CFT model [57,58] has the potential to help HCPs/clinicians understand, acknowledge and actively address and validate the fears and concerns of parents/caregivers of children with epilepsy and could help frame clinical consultations to address parental/caregiving fears and concerns. The provision of appropriate information, knowledge, meaningful clinical reassurance [79] and peer support may contribute to parents experiencing a greater sense of security (soothe) about managing daily life and the challenges of caring for their child with epilepsy.

Strengths and limitations

Although, overall, the studies were robust (e.g., had methodological coherence, appropriate research designs), the findings of this review are limited by poor or incomplete reporting in the studies, including incomplete reporting of type of epilepsy or type of seizure and/or severity of seizure and the child’s gender not always being reported. The transferability of the review findings is limited as most of the studies are based in Western/ developed countries and most participants were recruited via hospitals. This may be further exacerbated by the decision to exclude any non-English language studies. Another limitation is that although studies talk of parents/caregivers, there is a preponderance of mothers and typically parents/caregivers are considered separately. Although this could be considered a strength, the children with epilepsy represent a wide age range and a wide range of time since diagnosis. We did not include theses within the review which may be considered a limitation.

A strength of our scoping review is the engagement with parent/caregivers to frame our review question and inform subsequent thinking; this stage is often not undertaken but provided a meaningful contribution to the shaping of the work [84].

A further strength of the study lies in our engagement with parents who noted that our findings align with their lived experiences with one parent saying “I feel the conclusion [of the review] is spot on and awareness of the condition, as a whole, is massively lacking. This is something we as a family feel strongly about and it is vital that awareness is raised”.

Implications for research

Future research should actively consider the views of fathers and/or both parents/caregivers. There is also a need for future research to explore how knowledgeable, prepared and confident HCPs/clinicians (epilepsy nurse specialists/consultants etc) and other parents/caregivers are in supporting parents around many of these key issues. The CASTLE programme has recognised the need to explore parent/caregiver, child and clinician perspectives and the next stage is to explore clinicians’ perspectives. Additionally, future work could involve a collaboration between parents/caregivers and HCPs to explore the issues/topics for inclusion on a compassionate and collaborative agenda around relevant fears/concerns.

Implications for practice

The clinician priorities which can often shape the agendas for consultations may need to shift to encompass parents’/caregivers’ fears and concerns about things apart from actual seizures. Creating opportunities for parents to discuss issues with knowledgeable specialist epilepsy nurses and other HCPs and/or with other parents/caregivers could potentially mitigate factors that impact on parental/familial well-being and the child’s life and activities. Understanding the full range of parental fears and concerns about their child’s epilepsy may help HCPs to ensure they address the issues and/or signpost parents to relevant advice and support. These implications for practice would benefit from further research taking account of parents’ priorities and concerns.