Abiramy Fernando,1 Vinod Patel2
1 Paediatric Registrar, Warwick Medical School, Warwick University, Warwick, UK
2 Professorial Clinical Teaching Fellow: Diabetes and Clinical Skills; Hon Consultant in Endocrinology and Diabetes, Acute Medicine, Medical Obstetrics, Warwick Medical School, Warwick University, Warwick, UK
Address for correspondence: Dr Abiramy Fernando
Paediatric Registrar, Warwick Medical School, University of Warwick, Coventry, CV4 7AL, UK
E-mail: abiramy.fernando@nhs.net
https://doi.org/10.15277/bjd.2021.286
Background: Type 1 diabetes mellitus is one of the most common chronic childhood illnesses and, despite ongoing technological advances, hypoglycaemia remains an inevitable therapeutic risk. Hypoglycaemia results in unpleasant physiological outcomes, social embarrassment and – in extremis – life-threatening consequences. Overlying this inescapable clinical risk is a fear of this risk, ranging from fleeting to overwhelming, and substantially impacting the trajectory of diabetes.
Aim: The aim of this literature review is to identify, summarise and critically appraise works pertaining to the development, impact and management of paediatric fear of hypoglycaemia (FoH).
Methods: A search was conducted on Embase, MEDLINE and PsycINFO for studies published between 2000 and 2020, with cross-referencing searches for articles not detected in the original keyword search. Study quality was assessed using recognised tools, and relevant data were extracted systematically.
Results: Forty-three studies met the inclusion criteria. FoH was a moderate problem throughout the studies, increased by a history of hypoglycaemia and predisposition to psychological stress. There was conflicting evidence on the influence of age, diabetes duration, technology and parental demographics. Some studies showed a significant impact on glycaemic control and quality of life (QoL), more consistently for the latter. Only 13 intervention trials were included, showing mixed success with cutting-edge technology, and decent gains with psychological interventions.
Conclusions: FoH is clearly a ubiquitous issue among some families with type 1 diabetes. Prospective longitudinal studies are required to assess potential risk factors at diagnosis, monitor for the development of FoH at regular intervals, and enable a more comprehensive assessment of the long-term impact on glycaemic control and QoL. Further randomised controlled trials must demonstrate the value of technological and psychological therapies in order to make such interventions commonplace offerings for families suffering from intractable fear.
Br J Diabetes 2021;21:21:36-42
Key words: diabetes, hypoglycaemia, fear, HbA1c, quality of life
Type 1 diabetes mellitus (T1DM) is one of the most common chronic childhood illnesses, affecting 196 per 100,000 children aged 0–15 years in England and Wales.1 Despite rapid technological advances in diabetes therapy,2 hypoglycaemia remains the commonest acute complication of diabetes care.3 Intensive insulin therapy can increase hypoglycaemic frequency three-fold,4 and individuals with a <5-year T1DM duration experience on average 1.1 severe hypoglycaemic episodes per patient per year.5 Hypoglycaemia can result in unpleasant physiological symptoms, social embarrassment and – in extremis – life-threatening consequences. Overlying this inescapable clinical risk is a fear of this risk. This construct has been labelled a fear of hypoglycaemia (FoH) and can substantially impact the trajectory of diabetes. Individuals with strong FoH indulge in compensatory mechanisms to avoid hypoglycaemia, maintaining a ‘safe’ hyperglycaemia while carrying increased diabetes distress (DD) and poorer quality of life (QoL).
The aim of this literature review is to identify, summarise and critically appraise works pertaining to the development, impact and management of paediatric FoH. This will encompass examining FoH measurement tools, identifying predictive factors, exploring its impact and evaluating minimisation strategies. Prior works include a systematic review in parents of young children (PYC) containing six eligible studies6 and a broader review of children, adolescents and parents, comprising 16 studies.7 Although both highlighted the significance of FoH, its consequences were not fully explored, technology was less abundant, and paediatric behavioural trials non-existent. The current review aims to clearly delineate the impact of FoH on glycated haemoglobin (HbA1c) and QoL, underscoring the need for resource allocation. Moreover, diabetes care has been transformed by a decade of technological innovation, from continuous subcutaneous insulin infusions (CSII) and continuous glucose monitors (CGM) to sensor-augmented pump therapy (SAPT) and closed-loop systems, and the debate deserves reinvigorating.8-10
The research question was generated using the Population, Intervention, Comparator and Outcome (PICO) approach.11 The population comprised children and young people (CYP) aged 0–18 years with T1DM or their parents, and whether FoH influenced glycaemic control and QoL. A literature search was conducted on Embase, MEDLINE and PsycINFO. The bibliographies of retrieved papers were also reviewed. Letters to the editor, abstracts and scientific meeting proceedings were excluded. The search was restricted to English language publications from 2000 to 2020, to capture recent changes in technology (see Appendix 1, available online www.bjd-abcd.com, for full search strategy).
Titles and abstracts were examined for inclusion. All study designs meeting PICO parameters were eligible. Exclusion criteria included primarily adult-based studies, a failure to quantitatively assess FoH or either primary outcome. Included studies were critically appraised using recognised tools: the Centre for Evidence Based Medicine criteria for cross-sectional studies,12 the National Heart, Lung, Blood Institute checklist for pre-post prospective studies,13 and the Critical Appraisal Skills Programme checklist for randomised controlled trials (RCTs)14 and systematic reviews15 (Appendix 2 available online www.bjd-abcd.com).
Data extracted included study design, demographics, diabetes duration, insulin mode, HbA1c, FoH and QoL assessments, hypoglycaemia prevalence, pertinent results, strengths and limitations (Appendix 3 available online www.bjd-abcd.com). Due to differences in populations, treatment regimens and outcome measures, a meta-analysis was not conducted. Instead, a narrative synthesis is presented.
Search results
Of the 395 abstracts screened, 43 papers were included in the final analysis (see Figure 1).
The majority were cross-sectional studies (n=28), of which two datasets were used twice17-20 and three papers aggregated several studies.21-23 There were two literature reviews,6,7 five pre-post prospective studies and eight RCTs. Sample size ranged from 16 to 549 (mean 142) and 90% were of Western origin (Figure 2).
Eleven studies investigated parent-child dyads. Nineteen explored parental FoH, with 11 focusing on PYC, facing specific challenges of irregular eating and activities, difficulty matching insulin, greater aberrant glycaemia and subtleties in detection. Seven of 11 studies examining children’s FoH explored adolescents, confronting the complexities of puberty, subversion and peer influences.
Measurement of fear of hypoglycaemia
The Hypoglycaemia Fear Survey (HFS) is the most well-established measure assessing FoH, using a worry (HFS-W) and behaviour (HFS-B) subscale with 33 items graded from never to always on a Likert scale.24 The tool was modified to 25 items for parents (HFS-P)25 and revised for PYC (HFS-PYC).26 An adaptation for 6–18-year-olds also exists (HFS-C).27
The HFS-P demonstrates acceptable reliability with an internal consistency range of 0.88–0.91 for the HFS-W and 0.72–0.76 for the HFS-B.21 The HFS-B often displays slightly reduced internal consistency, registering appropriate hypoglycaemia avoidance strategies alongside inappropriate FoH-driven actions.7 Modified versions also show sufficient test-retest reliability.21 Although less used, the HFS-C has similarly been shown to have an internal consistency of 0.86 and good convergent validity.28 A key limitation of all HFS versions is the absence of established clinical cut-offs, making clinical interpretability challenging.7
The Children’s Hypoglycaemic Index (CHI) is a contemporary alternative, encompassing a fear, situation and behaviour subscale, demonstrating a good internal consistency of 0.89, decent test-retest reliability with a Pearson’s correlation coefficient of 0.76 and strong convergent validity among its various subscales. It was purposefully developed for children, explores more areas and comprises FoH-specific behaviours.29 However, it is less popular and requires further validation in practice.
Predictors of fear of hypoglycaemia
Hypoglycaemic frequency and severity is a key factor in FoH development.26,28 In a large Australian study of 325 parents of 8–18-year-olds, severe hypoglycaemia (SH) conveyed a 6.3 higher HFS-P score (p=0.004),30 while a Slovenian work linked SH with maternal hypoglycaemia preventative behaviours (r=0.25; p=0.03).31 SH also positively correlated with HFS-C helplessness scores (r=0.19; p=0.01) in an aggregated US study of 259 6–18-year-olds.22 SH clearly has a major role in the construct of FoH, although it can of course flourish irrespective of hypoglycaemic experience: in a large US study of PYC, recent SH was wholly unrelated to 549 HFS-P worry scores.32 Other studies show adolescent emergency glucose carriage (F=6.36; p<0.05)28 or diabetes management confidence (r=0.3; p<0.01) to be more predictive,33 highlighting the ability to deal with SH to be at least as important as experience of SH in the development of FoH.
A second hypothesis is that predisposition to stress, anxiety and depression contributes to FoH.34 Less mindful parenting was associated with higher HFS-P scores (p=0.006) for 421 Dutch parents,35 and a Norwegian study correlated the Hopkins Symptom Checklist-25 (HSCL-25) for depression and anxiety with HFS-P worry scales among 200 mothers (r=0.04; p<0.001) and fathers (r=0.28; p=0.006).19 Among CYP social anxiety and HFS-C scores positively correlated for North American boys (r=0.45; p<0.01) and girls (r=0.30; p<0.005),36 as did emotional disorders and HFS-B scores among Saudi adolescents.37 Of course, such psychological co-morbidities are also associated with certain sociodemographic factors, compounding vulnerability to FoH. For instance, parenting stress has been linked to having younger children, lower socioeconomic status and a non-Caucasian background, factors all also independently associated with FoH.38
The most noteworthy demographic variable was gender. Several international studies demonstrated significantly higher maternal HFS scores.18,19,26,31 Girls had higher HFS-C helplessness scores (F=4.33; p=0.039) than boys,22 and twice as high FoH scores (p<0.0001) in a 453-strong adolescent Swedish study.39 Few studies depicted no gender disparity.40 Age was also influential: parents of 6–11-year-olds had higher HFS-P scores than parents of children aged 0–5 years (p=0.003) or >12 years (p=0.003), perhaps reflecting care transition from parent to school,40 and adolescent age correlated with higher HFS-C social consequence scores.22 However, associations between age and FoH were inconsistent.32,41 The impact of technology was also indeterminate, ranging from higher HFS-P behaviour scores with multiple daily injections,19 and lower HFS-C worry scores with CSII (p<0.05),37 to no impact28,42 or moderate FoH encouraging CSII use.43
Impact of fear of hypoglycaemia
FoH is postulated to cause hypoglycaemia-avoidant behaviour, prolonged hyperglycaemia, poor glycaemic control and increased HbA1c levels. Hyper-vigilant parents admit to accepting higher target ranges where such vigilance is implausible,44 as do adolescents seeking to avoid humiliating public hypoglycaemia. Several studies confirmed significant associations between FoH scores and HbA1c.19,30,31,43 Others demonstrated no correlations between HFS-P,18,26,32 HFS-C17,37 and HbA1c. In some cases, despite high maternal HFS-B,45 or HFS-C maintain high blood glucose factor scales22 correlating with hyperglycaemia, there was no corresponding rise in HbA1c. It is clear that HbA1c is a multi-factorial derivation, often poorly reflective of everyday blood glucose excursions. More detailed glycaemic data are required to truly capture the impact of FoH on glycaemic control. Contrary to the initial hypothesis, FoH can also intensify diabetes control, negating any negative impact on HbA1c or even improving glycaemic control,21,23 although this was a far less common pattern.
The second key FoH impact is upon QoL, although few studies cite QoL as a primary outcome. It is challenging to deduce whether predisposition to stress, anxiety and depression increases FoH, or if FoH intensifies pre-existing psychological burden. In reality, this relationship is bi-directional and there is likely to be an element of reverse causality.34 Parents and children in the highest fear quartile have been shown to have lower scores on the Paediatric Quality of Life Inventory (PedsQL) by 20–22%,30 and significant associations have been demonstrated between FoH and DD in adolescent girls (p=0.044) and boys (p=0.026).39
Minimisation of fear of hypoglycaemia
The 13 paediatric intervention trials identified highlight the ambiguity of using technology to reduce hypoglycaemia risk and fear. The Juvenile Diabetes Research Foundation CGM RCT failed to exhibit appreciable reductions in HFS-P and HFS-C scores across 10 UK sites,46 while a smaller UK study of 16 adolescents did show HFS-P (98.69 vs 66.69; p<0.0021) and HFS-C (97.38 vs 59.75; p=0.003) reductions with 12 months’ CGM,47 as did an Australian crossover RCT evaluating remote monitoring mobile CGM.48 In a multicentre German observational study, CSII use for 6 months conferred significant reductions in HFS-P worry scores (d=0.4-0.6; p<0.01),49 with replicable results a decade later,50 and in Saudi Arabia, flash glucose monitoring improved adolescent HFS-C scores (p=0.0001).51 A multicentre crossover RCT involving Israel, Slovenia and Germany comparing an artificial pancreas system with SAPT for 4 nights demonstrated significant HFS-C worry reductions (1.04 vs 0.90; p=0.017),52 whereas a UK crossover RCT comparing closed loop systems with SAPT did not,53 nor did a multicentre Australian RCT comparing predictive low glucose management versus SAPT.54
A comprehensive adult literature review showcased blood glucose awareness training and cognitive behavioural therapy (CBT) as effective interventions.55 A US multisite RCT involving 258 adolescents evaluated the Flexible Lifestyles Empowering Change (FLEX) programme of motivational interviewing and problem- solving skills. Significant improvements were found in adolescent worry/helplessness criteria (−0.16; p=0.04), adolescent health- related QoL (3.18; p=0.009) and parents’ behaviours to maintain high blood glucose (−0.21; p=0.005).56 Another American intervention using video-based telehealth (REDCHiP) involved 36 parents of 2–6-year-olds. REDCHiP comprised a 10-week programme applying CBT principles to recognise FoH-related thoughts and behaviours, refining coping strategies and practising exposures to challenges. At 3 months there were significant reductions in HFS-PYC and DD scores.57
Main findings
FoH is a pervasive problem, dependent on a range of factors. Negative hypoglycaemic experience is clearly key, with psychological comorbidity serving as both a predictive and confounding factor. Greater female FoH prevalence undoubtedly reflects a higher female psychological burden with double the DD39 and greater anxiety levels,36,37 although paternal FoH is poorly represented with the only dedicated study displaying low FoH and state anxiety.58 FoH often results in deteriorating glycaemic control, which is sometimes reflected in increased HbA1c levels. The impact of FoH on QoL is also more nuanced, as innumerable variables contribute to QoL, not least of which is chronic illness itself.59
Technology has a definitive role in minimising FoH, which is most beneficial in conjunction with psychological gains. Successful intervention studies reveal significant reductions in PedsQL,49 parental health-related QoL, stress and anxiety, alongside FoH reductions.48 Psychological intervention is clearly vital, but requires significant buy-in. A UK pilot of problem-solving workshops highlighted significant recruitment issues: although over 90% of the 89 families approached had high HFS-P scores, only 25% participated, citing reluctance to miss school, lack of time, interest or travel difficulties.60 Lessons must be learnt for future directives and further statistically powered RCTs are needed to confirm the validity of this approach.
Strengths and limitations
The majority of papers were cross-sectional studies, relatively quick, low-cost undertakings, useful in displaying prevalence, associations and new hypotheses, but unable to establish causality or temporality. Only seven studies performed power calculations to justify sample size; others were likely woefully underpowered. Inter-study variability also rendered some comparisons or aggregations redundant. For instance, a third of studies lacked a definition for SH, definitions varied widely, and most SH was self-reported. Only four intervention trials listed FoH as a primary outcome, nevertheless 92% provided significant p values with precise confidence intervals. Sadly, all lacked a cost-benefit analysis (Appendix 2).
Although FoH measurement was largely comparable and robust, with 93% of studies using the psychometrically strong HFS, this questionnaire is subject to recall bias, requires literacy, self- assessment and abstract reasoning. Age-specific considerations include the ability of younger children to hypothecate, adolescents to be candid and parental engagement in diabetes care. The impact of FoH was chiefly assessed upon HbA1c and QoL. The validity of the former was marred by historic clinic records, different laboratories, self-report35 and missing data.45 It is also likely that time spent in range is a more useful marker than HbA1c. QoL was assessed using an array of established tools, limiting comparability, and was coloured with recall bias.
Selection bias was a fundamental limitation: most recruited opportunistically from diabetes clinics or camps, 22 were restricted to single centres and only a handful accessed national registries.32,35,39 Participants were self-selected by virtue of attending clinic, answering calls or adverts, reflecting a motivated cohort. Further commitment involved questionnaire completion, regular self-monitoring of blood glucose or embracing technology. Response rates across 27 studies ranged from 21% to 96% (mean 61%). Engaged respondents generally revealed better glycaemic control than non- respondents,30,31,39,57 with a mean study participant HbA1c of 66.6 mmol/mol and CSII use of 5–86%, often deviating markedly from UK rates of 36.7%.1 Studying populations with better glycaemic control potentially skews the FoH burden and its confounders.
Reviewing only English language publications delivered populations fairly reflective of the UK. Middle Eastern studies relied on questionnaire translation and back-translation,17,18,37,51 as did many European studies.19,20,31,49,50 This may have introduced inaccuracies and cultural inconsistencies. Study cohorts reflected narrow socioeconomic groups: 20 of 23 studies describing ethnicity were 71–97% Caucasian, 15 had a 69–98% married population and 22 demonstrated higher parental education, employment or income (Appendix 3). This diminishes the wider applicability of the results while highlighting the time, interest and literacy often decisive in study participation. Future studies need selection processes which overcome these biases. Mothers represented 52–98% of parent participants (mean 80%) across 20 studies, excluding exclusively maternal or paternal studies.45,58,59 Achieving gender parity is challenging, as mothers are usually the primary caregivers whereas fathers undertake <20% of diabetes-related tasks.58 It is nevertheless important that future studies are more representative.
Implications for future research and practice
There has been a substantial body of work evaluating the scope of paediatric FoH, but to truly capture the natural history of an often transient phenomenon, large-scale prospective longitudinal studies are required. An assessment of FoH should include the validated HFS and an objective psychological evaluation. The outcome of glycaemic control should be broadened to include CGM data, acute and secondary complications. QoL should be assessed by both subjective questionnaires and objective psychological appraisal. To limit selection bias, studies must aim to include both parents of all patients within a named diabetes centre, with efforts to minimise language and travel barriers. Further statistically powered RCTs must confirm the validity and applicability of interventions. Awareness of FoH should be raised among local paediatric diabetes multidisciplinary teams, CYP and their parents, with a view to including HFS-P, HFS-PYC and HFS-C surveys within the annual diabetes review so at-risk families can be offered appropriate interventions.
This review indicates that FoH is an important issue among CYP with T1DM and their parents. There are several factors involved in the development of FoH. Personal experience of hypoglycaemia and psychological vulnerability are core features in the construct, but the weight of these factors depends on a host of other sociodemographic variables. The true causality and burden of FoH can be better established in prospective longitudinal studies, assessing these potential risk factors at diagnosis and monitoring for the development of FoH at regular intervals. Significant FoH can invariably impact diabetes management and glycaemic control; longitudinal results with CGM data will enable a subtler evaluation of this relationship. Study spans over decades can also assess the psychological burden of FoH more comprehensively than snapshot cross-sectional data. Although such studies are costly and susceptible to high drop-out rates, they are necessary to accurately define the long-term impact of FoH. This enables at-risk individuals to be identified more readily, and intervention measures to be better tailored. Despite a recent expansion in paediatric FoH intervention trials, numbers are still small. A greater volume of such trials, with larger study numbers, are desperately needed to demonstrate the value of technological and psychological therapies in order to make such interventions commonplace offerings for families suffering from intractable fear.
Conflict of interest None.
Author contributions AF conducted the literature review and wrote the first draft. VP reviewed the content and suggested amendments which AF incorporated.
Funding None.
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