In addition to providing a descriptive review, this article also presents new findings regarding the assessment of FoH in children at different age levels and in parents whose Type 1 children differ in age and developmental stage. By aggregating separate datasets from previous studies in our laboratory that included measures of FoH in Type 1 youths and their parents, it was possible to investigate several important questions that require information on a large number of children with a broad range in age. These included questions concerning age effects on level of FoH in children and adolescents, as well as the ability of younger children to provide reliable and valid self-reports of this fear. Before these findings are presented, this article will review the existing literature on pediatric FoH, beginning with an exploration of the problem of hypoglycemia in Type 1 diabetes and it is especially problematic impact on Type 1 diabetes in children.

In youths, as in adults, hypoglycemic episodes are typically triggered by behaviors that result in a mismatch in insulin, food and physical activity. Regulation of food intake and physical activity in relation to insulin concentrations are especially problematic in children and adolescents. Eating can be unpredictable in the amounts and timing of carbohydrate consumption, such as in toddlers and preschool children who can resist food intake at times and adolescents who may engage in more snacking and social food consumption. Physical activity can also occur unpredictably in youths. The most common adverse consequence of exercise in individuals with Type 1 diabetes is falling glucose levels [8], therefore vigorous physical activity is a major risk factor for significant hypoglycemia [9]. Unfortunately, some youth and their parents may attempt to decrease this risk by over-consumption of carbohydrates before, during and after exercise [10].

For youths, the possible negative effects of SH on neurocognitive functioning also make hypoglycemia especially problematic. There is mixed evidence on whether recurrent episodes of SH have long-lasting negative cognitive effects in both adults and children with Type 1 diabetes [11,12]. However, patients diagnosed at a younger age (e.g., 4 or 5 years of age), as well those from lower socioeconomic backgrounds, may be at greater risk [13–15]. However, these findings are poorly understood owing to the number of confounding variables in addition to SH that may affect cognitive function in children with Type 1 diabetes, including duration of diabetes and frequency of diabetic ketoacidosis. Meta-analyses have concluded that children with Type 1 diabetes experience mild cognitive impairments compared with nondiabetic controls, specifically on measures of general intelligence, attention, visuospatial abilities and motor speed [16,17]. But these differences may be related to hyper- not hypo-glycemia [12,18]. In addition, there is evidence that SH may be related to deficits in short-term verbal memory, but results are inconsistent and warrant further research [16,17,19].

Research on continuous glucose monitoring (CGM) has highlighted the fact that nocturnal hypoglycemia is particularly worrisome for children, as it can lead to delayed treatment or may go undetected altogether [20]. Early CGM studies found high incidence rates of nocturnal hypoglycemia in the pediatric population, with estimated rates ranging from 14–47% [21,22]. In addition to CGM studies, the DCCT found that more than half of SH episodes occurred during the night, and Davis and colleagues reported that 75% of youth’s SH episodes occurred at nighttime [6,7]. The risk of nocturnal hypoglycemia is particularly concerning for parents, who actively engage in night time management of their children’s diabetes. For example, parental anxiety about nocturnal hypoglycemia often results in increased monitoring of BG levels overnight, which can cause increased parenting stress and anxiety [23], and in extreme cases may lead parents to keep their child’s BG levels higher at night.

In addition to nocturnal hypoglycemia, episodes of SH occurring at school or in other places where the child is supervised by adults with limited knowledge about hypoglycemia or its treatment is a significant concern for parents. A study found that while the most common fear reported by parents concerning hypoglycemia was the occurrence of nocturnal episodes, the next most common fear was the child experiencing hypoglycemia when away from the parent [24]. Research on parental perspectives regarding their children’s diabetes management at school is sparse but suggests that the majority of parents perceive it to be inadequate, as school personnel are often not formally trained in diabetes management [25]. School personnel have also reported concerns about liability, which prevents them from providing adequate routine care and emergency treatment, such as administering glucagon injections in cases of SH [26].

Adequate reliability for the PHFS has been reported by several studies, with internal consistency ranging from 0.72 to 0.76 for the PHFS-B and 0.88 to 0.91 for the PHFS-W [29,55]. In addition to the PHFS created by our research group, other researchers have independently modified the original HFS to assess parental actions to prevent hypoglycemia in their children, as well as their concerns about their children experiencing hypoglycemia [54]. A more recent study [56] modified the survey for assessment of FoH in parents of very young children with Type 1 diabetes, including toddlers (e.g., ‘Feed my child as soon as I feel or see the first signs of a low blood sugar.’). These modified parent versions have retained good internal consistency and test–retest reliability and they have yielded scores that were comparable to other published data [54,56].

Compared with the parent and adult versions of the HFS, there is less research on the psychometric properties of the CHFS, but the available findings indicate adequate reliability. In a recent study of FoH in adolescents with Type 1 diabetes, Cronbach’s αs for the CHFS demonstrated adequate internal consistency for the CHFS-Total score and the CHFS-W (0.86 and 0.91, respectively), with lower internal consistency for the CHFS-B (0.54) [29]. In another independent modification of the adult HFS for a study of FoH in Type 1 children attending diabetes camp [52], the scale showed adequate internal consistency (Cronbach’s α coefficients 0.85, 0.64 and 0.88 for the CHFS-Total, CHFS-B and CHFS-W, respectively) and test–retest reliability.

Early studies using the PHFS found higher levels of FoH in mothers whose children experienced loss of consciousness owing to hypoglycemia, as well as those who were highly distressed by their children’s episodes during the night or in social situations [55]. There is also some evidence showing that maternal FoH is higher for those with children on multiple daily injections compared with an insulin pump [49,57,58]. In a study of mothers of younger children (2–8 year olds), maternal FoH did not correlate with child frequency of SH episodes, although this may have been attributable to an overall low rate of SH in the sample [56]. However, a study of mothers of adolescents with Type 1 diabetes also found no relationship between frequency of SH in their children and FoH. Instead, the only predictor was mothers’ belief about whether or not their adolescent always carried fast-acting carbohydrate for hypoglycemic treatment [29]. A total of two studies have investigated correlates of FoH in adolescents with Type 1 diabetes, both finding that, like adults, frequency of SH predicted FoH [29,54]. Also similar to findings in adults, FoH in adolescents was associated with trait anxiety [29]. No published studies have yet investigated predictors of FoH in younger children.

Only one previous study has compared levels of FoH in mothers of younger children and those of older children and found no significant differences in level of FoH [56]. However, maternal FoH does appear to be significantly higher than paternal FoH, although it remains to be seen if this difference is clinically as well as statistically different [56,58]. Perhaps not surprisingly, more than one study has found that levels of FoH in mothers of youths with Type 1 diabetes are significantly higher than the levels observed in adult patient populations [55,56].

As in adults with Type 1 diabetes, there is an assumption that extreme FoH in either the parent or child can interfere with optimal diabetes management and control. That is, families with very high FoH may engage in more diabetes management behaviors to avoid hypoglycemia, which may lead to more frequent hyperglycemia. However, studies have, again, yielded inconsistent results. Several studies have investigated the relationship between FoH and diabetes control, based on the assumption that, if more FoH leads to more frequent hyperglycemia, HbA1c levels should be higher. Although some studies have not found an association between maternal or youth FoH and HbA1c levels [29,54,56,59], others have reported a positive correlation between mothers’ FoH and their children’s glycemic control [55,58]. Patton et al. reported a correlation between higher PHFS-B subscale scores and youth’s HbA1c levels in mothers of young children with Type 1 diabetes, suggesting that parents of children in poorer metabolic control more frequently engage in behaviors to prevent hypoglycemia [56].

We have recently attempted to address these questions by aggregating CHFS and PHFS data from several separate studies conducted in our laboratory over the past decade. In addition to CHFS and PHFS data, each of these studies also included demographic (age of youth and gender) and clinical (HbA1c level and duration of diabetes) data, as well as other psychological measures relevant to HFS validity (e.g., anxiety measures, which are described in detail later). The total aggregated sample included 259 youths with Type 1 diabetes and 250 parents. Youths had a diagnosis of Type 1 for at least 1 year (mean: 5.24; standard deviation [SD]: 3.28 years) and ranged in age from 6 to 18 years (mean: 10.56; SD: 3.31 years). Youths (45.5% female) were divided into three age groups as follows: 6–8 years old (n = 85), 9–11 years old (n = 95) and 12–18 years old (n = 79). Over a third of the youths used insulin pump therapy (38%) and average HbA1c was 8.01% (0.97). For the parent sample, the majority were mothers (81.3%) and Caucasian (88%) and generally highly educated (mean education: 15.15; SD: 2.77 years).

In spite of the potential scientific and clinical utility of the PHFS and CHFS, more research is needed to increase our understanding of both the construct of FoH in pediatric diabetes and its impact on disease management and outcome. The new findings presented in this article, based on a large aggregated dataset, highlight the importance of investigating FoH across age ranges and developmental stages of youth with Type 1 diabetes and their parents. Large datasets are also needed for factor analysis studies, which can help to clarify the underlying domains of FoH that are measured by the PHFS and CHFS. Most previous studies in this area, with only a few exceptions [56,58], have focused on maternal FoH and we know little about paternal FoH. Perhaps most importantly, large datasets are needed to establish normative levels of FoH. Given the potential danger of hypoglycemia, some level of fear is adaptive and appropriate. Therefore, it is important to identify CHFS and PHFS scores reflecting a healthy level of concern, as well as those that indicate possible problematic levels of FoH.

The construct of FoH in pediatric patients and their parents has received relatively limited scientific attention over the past decade, which is somewhat surprising given its potential clinical significance and the apparent increase in Type 1 diagnosis in younger children in many parts of the world [67,68]. A recent review of the literature on FoH in parents of children under 12 years of age found only eight published studies that met their liberal criteria for inclusion [69]. That review and the present one, demonstrate that the majority of published studies have significant methodological limitations including: cross-sectional designs, solely descriptive analyses, limited sample sizes, narrow youth age ranges and a lack of outcome measures critical for testing hypotheses regarding the impact of FoH on diabetes management and outcome. More sophisticated research is needed, particularly longitudinal studies to follow families over time as they confront and are affected by hypoglycemia-related experiences. Such an approach would help shed light on factors influencing the development of FoH, as well as the impact of FoH on diabetes treatment and control. Like other types of stimulus-specific anxiety, FoH can suddenly increase with exposure to highly aversive and threatening experiences with hypoglycemia. However, it is still unclear exactly what characteristics of a hypoglycemia episode are most likely to lead to increased FoH. However, studies have found higher levels of FoH in parents with a history of the child passing out or having a seizure due to hypoglycemia and other types of distressing events. This suggests that families who have recently experienced a traumatic hypoglycemic episode may be most vulnerable to increased FoH and should be assessed for reactions that may interfere with quality of life or optimal diabetes treatment. FoH should also be assessed in families characterized by high levels of trait anxiety, even though the relationship between this personality trait and FoH in parents and younger children remains unclear. These families may need assessment even if they have not yet experienced traumatic hypoglycemic episodes since individuals very high in trait anxiety are predisposed to anticipatory anxiety, or anxiety about an event even before it actually occurs.

A noteworthy study testing an intervention to reduce SH in youth provides intriguing evidence that positive outcomes do not necessarily require highly complex programs or technology [60]. This study tested the widespread distribution of educational and training materials, including videotapes, aimed at teaching families appropriate and effective strategies for preventing hypoglycemia. The rate of SH in these families was subsequently cut almost in half and this reduction was maintained over several years. These results suggest that we may be missing opportunities to develop and implement interventions that are effective from an outcome and cost perspective at reducing the problem of hypoglycemia and its negative consequences, including FoH. In addition to interventions to reduce hypoglycemia risk, there is also a need for interventions that directly target extreme and problematic FoH, which may arise independent of actual hypoglycemia risk or history.

Looking into the future, another area of emerging importance will be FoH in pediatric Type 2 diabetes. Currently youth with Type 2 diabetes are typically managed with oral antihyperglycemic medications and the most pressing clinical concern is reducing chronic hyperglycemia. However, it is likely that over time it will become more common to use insulin regimens in this population in order to improve diabetes control. As this occurs, the problem of hypoglycemia and FoH will no doubt also increase.

Finally, an important area for future development will be the investigation of FoH as a global problem in pediatric Type 1 diabetes. There is a larger body of literature on FoH in adults with both Type 1 and Type 2 diabetes across other countries, including Germany, The Netherlands, Slovenia, the UK, China, Sweden and Turkey [73–78]. In pediatric diabetes, there is some encouraging growth in cross-cultural studies. For example, results from a recent Norwegian population-based study demonstrated that parental FoH was prevalent and was related to both increased emotional distress in parents and poorer glycemic control in children [58]. Other ongoing research projects are looking at FoH in youth with Type 1 diabetes and their parents in additional countries, including Turkey, Iran, Germany and the UK, and findings from these studies will soon be added to our knowledge base. This research will further advance our understanding of the global relevance of FoH and provide the opportunity to identify similarities and differences across countries and cultures.