2023 Volume 70 Issue 9 Pages 875-882
Primary caregivers of children with type 1 diabetes mellitus (T1DM) are prone to negative emotions. This study explored the anxiety status of the caregivers and analyzed the related factors. In this prospective study, 245 primary caregivers of T1DM children who were reexamined in the outpatient clinic of Children’s Hospital affiliated to Zhengzhou University between April 2020 and Sep 2022 were surveyed with a questionnaire and the Hamilton Anxiety Rating Scale (HAMA). The detection rate of anxiety symptoms in T1DM primary caregivers was 21.2%, with a total score of HAMA score of 11.74 ± 2.50. There were significant differences between the anxiety and non-anxiety groups in treatment method, HbA1C to standard (≤7.0%), severe hypoglycemia in the last 1 year and the number of adolescent cases (χ2 = 15.798, p = 0.000; χ2 = 4.197, p = 0.040; χ2 = 5.291, p = 0.021; χ2 = 14.279, p = 0.000). Multivariable logistic regression analysis showed that insulin pump treatment, HbA1C to standard (≤7.0%) and adolescence were associated with anxiety in primary caregivers (OR = 4.040, 95%CI 1.969–8.289, p = 0.000; OR = 0.472, 95%CI 0.237–0.955, p = 0.037; OR = 2.952, 95%CI 1.495–5.831, p = 0.002). Pediatric endocrine care should pay more attention to the anxiety of the caregivers of adolescent T1DM children treated with insulin pumps while helping the children manage their disease.
TYPE 1 DIABETES MELLITUS (T1DM) is the most common type of childhood and adolescent diabetes mellitus and is an autoimmune disease mediated by T lymphocytes that selectively destroy the islet β cells, leading to an absolute lack of insulin secretion [1-3]. The incidence of T1DM in children and adolescents is steadily increasing, showing a great variation across countries and age groups. Based on relevant surveys, the incidence of T1DM in children <14 years of age was 1.93/100,000 in China in 2010–2013, and the 0–4 years old group had the fastest increasing incidence [4-7]. At present, T1DM treatment still involves a daily subcutaneous injection of insulin or insulin pump, diet and exercise management, blood glucose monitoring, and diabetes education. As there is no radical treatment plan, lifelong treatment is needed [8]. If blood glucose is not well controlled in these children, about half of them will develop various complications within the course of the disease within about 12 years [9, 10], putting pressure on caregivers since caregivers do not want harm to occur to their children [11]. In addition, patients with T1DM require adapted nutrition, exercise, medicines, monitoring, and extensive medical knowledge from the caregivers [12, 13]. T1DM treatment also requires expenses, and the whole family need to bear a greater economic burden [14].
Due to the limitation of self-care ability in these children, they are dependent on help from their caregivers [11]. The primary caregivers provide daily life assistance outside and in the hospital and protect the rights and interests of the patients during hospitalization [15, 16]. Long-term treatment for children with T1DM makes them prone to psychosocial problems, such as hyperactivity, aggression, anxiety, depression, loneliness tendency, and social withdrawal [17-21]. As a support system for children requiring the treatment for chronic diseases, the primary caregivers of T1DM require more energy, spirit, and economic resources [22, 23]. The multiple long-term stress and concerns related to chronic complications can easily lead to negative emotions among the caregivers, thus hindering the care of children with T1DM and eventually resulting in poor blood glucose control [24-26]. Thus, the negative emotions of the primary caregivers cannot be ignored.
At present, there are few studies on the mental health status of the primary caregivers of T1DM children, and they are limited to the study of anxiety status, with little analysis of relevant influencing factors [27-30]. Anxiety is an unpleasant experience of external events or internal feelings involving a series of emotions of the same nature but varying degrees. The lightest symptoms are anxiety and worry, followed by fear and panic, while the heaviest one is extreme terror. The manifestations include subjective nervous experience, behavioral motor anxiety, and autonomic nerve arousal symptoms. Herein, we discussed the current situation and influencing factors of anxiety among the primary caregivers to provide a theoretical reference for their mental health intervention, which is conducive to the comprehensive management of T1DM children.
The primary caregivers of children with T1DM aged 2–18 were selected as the study participants between April 2020 and Sep 2022. The inclusion criteria were (1) parents or immediate relatives of children with T1DM, with continuous care time of more than 1 month, and (2) certain reading and understanding ability, informed consent, and voluntary participation. The exclusion criteria were (1) communication barriers, (2) chronic somatic diseases affecting the quality of life, (3) mental diseases, or (4) major stress events that occurred in the family over the recent 3 months. This study was approved by the Ethics Committee of Henan Children’s Hospital (2020-NMF-016), and all participants provided written informed consent.
QuestionnaireThe questionnaire was conducted anonymously. The investigators, who were the medical staff of Henan Children’s Hospital, participated in the survey after passing the training. The purpose and significance of the survey, questionnaire filling, and quality control were explained to the participants. After completing the questionnaires, the investigators collected them on the spot. The questionnaires were uniformly coded and processed. The criteria for effective questionnaires were (1) no missing answers, (2) answers of the whole questionnaire were not the same, (3) selected items in the whole questionnaire were irregular, and (4) one answer for each question. A total of 255 questionnaires were distributed; five had missing answers, and five had two answers to two questions. Finally, ten invalid questionnaires were excluded, and 245 valid questionnaires were recovered, with an effective recovery rate of 96.1%. In order to validate the questionnaires, the primary caregivers participating in the survey were interviewed by telephone within 1 week after the survey. The questionnaire information was investigated again, and those with a consistency rate of <90% were included.
ToolsA questionnaire on general information was designed by the researchers, and it included the following contents: 1) child patient: gender, age, age of onset, course of the disease, treatment method, glycosylated hemoglobin level, whether in adolescence, whether to wear dynamic blood glucose monitoring, etc.; 2) primary caregiver: gender, age, education level, spouse age, occupation, annual family income, etc.
The Hamilton Anxiety Rating Scale (HAMA, sometimes termed HARS) was created in 1959. It was one of the first rating scales to measure the severity of perceived anxiety symptoms. It is considered one of the most widely used rating scales. It has been used as a benchmark for more recently devised scales. It consists of 14 symptom defined elements. It uses the 5-level rating method of 0 to 4 points. The total score is 0–56, and the anxiety level can be divided as follows: <7 means no anxiety, 7–14 means possible anxiety, 15–21 means certain anxiety, 21–29 means obvious anxiety and >29 means severe anxiety. Score 14 is generally the critical value. The reliability coefficient (Cronbach’s α) of HAMA is 0.93 after localization in China, and the correlation coefficient to the total score of HAMA was 0.36 (p < 0.05) [31].
Statistical analysisSPSS 22.0 was used for statistical analysis. The disease course, age of onset, and other data conforming to the normal distribution were expressed as mean ± standard deviation, and the categorical data, such as gender and treatment method, were expressed as the number of cases (percentage). The t-test was used to compare the differences in continuous data in line with the normal distribution between the two groups. The categorical data were tested by the χ2 test. Multivariable logistic regression analysis was used to analyze the factors related to the anxiety of the primary caregivers. Odds ratio (OR) and 95% confidence interval (95% CI) were used to express the correlation strength of factors. p < 0.05 was considered statistically significant.
A total of 245 children with T1DM and their primary caregivers were investigated, including 110 boys, with an average age of 9.24 ± 3.64 years and a course of 3.84 ± 2.55 years. 110 patients were treated with insulin pumps, 135 with insulin pens, 202 with dynamic blood glucose monitors, and 148 reached the HbA1c standard. Among the primary caregivers, there were 147 mothers and 98 fathers with an annual family income (85 cases) over 50,000 CNY (Table 1).
| T1DM children | |
| Item | Result |
| Boys (n (%)) | 110 (44.89%) |
| Age (years)) | 9.24 ± 3.64 |
| Age of onset ((mean ± SD) years) | 5.41 ± 2.92 |
| Course of disease ((mean ± SD) years) | 3.84 ± 2.55 |
| Ketoacidosis at onset (n (%)) | 179 (73.06%) |
| Severe hypoglycemia in the last 1 year (n (%)) | 140 (57.14%) |
| Treatment | |
| Insulin pump (n (%)) | 110 (44.90%) |
| Insulin pen (n (%)) | 135 (55.10%) |
| Dynamic glucose monitor (n (%)) | 202 (82.44%) |
| Annual times of reexamination ((mean ± SD) times) | 2.36 ± 1.03 |
| HbA1C ((mean ± SD) %) | 7.04 ± 1.12% |
| HbA1C to standard (≤7.0%) (n (%)) | 148 (60.4%) |
| In adolescence (n (%)) | 91 (37.14%) |
| At school age (n (%)) | 155 (63.27%) |
| Family history of diabetes (n (%)) | 82 (33.47%) |
| Family history of cardiovascular disease (n (%)) | 117 (47.76%) |
| Primary caregiver for T1DM children | |
| Item | Result |
| Mother as primary caregiver (n (%)) | 147 (60.00%) |
| Father as primary caregiver (n (%)) | 98 (40.00%) |
| Below high school education of primary caregiver (n (%)) | 88 (35.92%) |
| Mean age of primary caregivers ((mean ± SD) years) | 35.40 ± 5.72 |
| Mean age of primary caregiver spouses ((mean ± SD) years) | 40.20 ± 12.45 |
| Primary caregiver occupation | |
| Workers and agricultural production personnel (n (%)) | 41 (16.73%) |
| Business and service people (n (%)) | 31 (12.65%) |
| Staff of government agency, enterprises and institutions (n (%)) | 33 (13.47%) |
| Professionals (n (%)) | 22 (9.98%) |
| Self-employed (n (%)) | 34 (13.88%) |
| Other or unemployed (n (%)) | 84 (34.29%) |
| Annual household income above 50,000 CNY (n (%)) | 85 (34.69%) |
T1DM: type 1 diabetes mellitus, HbA1C: glycosylated hemoglobin, CNY: China Yuan.
Among the 245 primary caregivers of T1DM children, 52 (21.2%) had mild anxiety, no obvious anxiety and serious anxiety. The total HAMA score of the primary caregivers was 11.74 ± 2.50.
Comparison of the clinical data between the anxiety and non-anxiety groupsThe significant differences were found in treatment method, HbA1C to standard (≤7.0%), and whether there was severe hypoglycemia in the last 1 year, and whether in adolescence (χ2 = 15.798, p = 0.000; χ2 = 4.197, p = 0.040; χ2 = 5.291, p = 0.021; χ2 = 14.279, p = 0.000) in primary caregivers of T1DM children in the anxiety and non-anxiety groups. There were no significant differences in age, gender of primary caregivers, age of spouse, age of the child, age of onset, course of the disease, HbA1C, absence of ketoacidosis at onset, or whether to wear a dynamic glucometer or not (p > 0.05) (Table 2).
| Item | Anxiety group (52) | Non-anxiety group (193) | χ2/t | p |
|---|---|---|---|---|
| Age of children ((mean ± SD) years) | 9.19 ± 3.49 | 9.26 ± 3.68 | –0.121 | 0.904 |
| Age of onset ((mean ± SD) years) | 5.38 ± 2.58 | 5.37 ± 2.98 | –0.101 | 0.919 |
| Disease of course ((mean ± SD) years) | 3.81 ± 2.25 | 3.85 ± 2.63 | 0.091 | 0.927 |
| HbA1C ((mean ± SD) %) | 7.29 ± 1.10 | 6.97 ± 1.12 | 1.816 | 0.071 |
| Children, boy (n (%)) | 20 (38.46) | 90 (46.63) | 1.105 | 0.293 |
| Ketoacidosis at onset (n (%)) | 13 (25.00) | 53 (27.46) | 0.126 | 0.723 |
| Severe hypoglycemia in the Last 1 year (n (%)) | 15 (28.85) | 90 (46.63) | 5.291 | 0.021 |
| Annual times of reexamination ((mean ± SD) times) | 2.52 ± 1.02 | 2.32 ± 1.03 | 1.237 | 0.218 |
| Treatment of insulin pump (n (%)) | 36 (69.23) | 74 (38.34) | 15.798 | 0.000 |
| Dynamic glucose monitoring (n (%)) | 13 (25.00) | 30 (15.54) | 2.531 | 0.112 |
| HbA1C to standard (≤7.0%) (n (%)) | 25 (48.07) | 123 (63.73) | 4.197 | 0.040 |
| Number of children in adolescence (n (%)) | 31 (59.62) | 60 (31.09) | 14.279 | 0.000 |
| Number of children at school age (n (%)) | 37 (71.15) | 118 (61.14) | 1.768 | 0.184 |
| Family history of DM (n (%)) | 19 (36.53) | 63 (32.64) | 0.279 | 0.597 |
| Father as primary caregiver (n (%)) | 24 (46.15) | 74 (38.34) | 1.042 | 0.307 |
| Age of primary caregivers ((mean ± SD) years) | 35.88 ± 5.68 | 35.27 ± 5.74 | –0.687 | 0.493 |
| Age of primary caregiver spouse ((mean ± SD) years) | 39.54 ± 13.19 | 40.38 ± 12.28 | –0.431 | 0.667 |
| High school education or below of primary caregivers (n (%)) | 23 (44.23) | 65 (33.68) | 1.982 | 0.159 |
| High school education or below of primary caregiver spouse (n (%)) | 27 (51.92) | 34 (17.62) | 3.118 | 0.077 |
| Occupation of primary caregiver (n (%)) | 7.559 | 0.182 | ||
| Worker and agricultural worker | 8 (15.38) | 33 (17.10) | ||
| Business and service practitioner | 6 (11.54) | 25 (12.95) | ||
| Employee of state organs, enterprises and institutions | 12 (23.08) | 21 (10.88) | ||
| Technical professional | 2 (3.85) | 20 (10.36) | ||
| Self-employed | 5 (9.62) | 29 (15.03) | ||
| Others or unemployed | 19 (36.54) | 65 (33.68) | ||
| Occupation of primary caregiver spouse (n (%)) | 8.709 | 0.121 | ||
| Worker and agricultural worker | 6 (11.54) | 27 (13.99) | ||
| Business and service practitioner | 8 (15.38) | 34 (17.62) | ||
| Employee of state organs, enterprises and institutions | 2 (3.85) | 26 (13.47) | ||
| Technical professional | 6 (11.54) | 30 (15.54) | ||
| Self-employed | 18 (34.62) | 54 (27.98) | ||
| Others or unemployed | 6 (11.54) | 26 (13.47) | ||
| Annual household income above 50,000 CNY (n (%)) | 34 (65.38) | 126 (65.28) | 0.000 | 0.989 |
| PSQI, (mean ± SD) | 5.90 ± 2.946 | 6.00 ± 2.96 | –0.208 | 0.835 |
| APGAR, (mean ± SD) | 6.06 ± 1.45 | 6.20 ± 1.38 | –0.663 | 0.508 |
| Time of medium- to high-intensity physical exercise of primary caregiver per week (n (%)) | 1.531 | 0.465 | ||
| ≤150 minutes | 5 (9.62) | 11 (5.70) | ||
| 150 to 300 minutes | 21 (40.38) | 92 (47.67) | ||
| ≥300 minutes | 26 (50.00) | 90 (46.63) |
DM: diabetes mellitu, PSQI: Pittsburgh sleep quality index, APGAR: Family adaptation, partership, growth, affection, resolve.
The anxiety of caregivers of T1DM children was taken as the dependent variable (normal = 0, anxiety = 1). Multivariable logistic regression analysis was carried out using the child’s gender and the facts with significant differences (treatment method, HbA1C to standard, severe hypoglycemia in the past 1 year, adolescence) as the possible influencing factor of anxiety. The independent variables were screened by stepwise regression, and collinearity was excluded among the variables. The inclusion criterion of variables was α = 0.05, and the exclusion criterion was α = 0.10. The results showed that treatment with insulin pump, HbA1C to standard and adolescence were associated with anxiety (OR = 4.040, 95%CI 1.969–8.289, p = 0.000; OR = 0.472, 95%CI 0.237–0.955, p = 0.037; OR = 2.952, 95%CI 1.495–5.831, p = 0.002) (Table 3).
| Research variable | β | Standard error | OR | 95%CI | p |
|---|---|---|---|---|---|
| Boy | 0.115 | 0.358 | 1.122 | 0.556–2.263 | 0.748 |
| Treatment of insulin pump | 1.396 | 0.367 | 4.040 | 1.969–8.289 | 0.000 |
| HbA1C to standard (≤7.0%) | –0.750 | 0.359 | 0.472 | 0.237–0.955 | 0.037 |
| Severe hypoglycemia in the last 1 year | 0.440 | 0.371 | 1.553 | 0.751–3.213 | 0.235 |
| Adolescence | 1.083 | 0.347 | 2.952 | 1.495–5.831 | 0.002 |
HbA1C: glycosylated hemoglobin
These studies suggested that the primary caregivers of T1DM children had the high levels of anxiety in Khemakhem and Whittemore et al. [27, 29]. Our study showed that 21.2% of the primary caregivers of children with T1DM have mild anxiety, but no obvious anxiety and serious anxiety. In 2017, Han et al. [32] conducted a SAS assessment on 100 primary caregivers of T1DM children and reported that the anxiety standard score of the main caregivers of children with T1DM was 49.2 ± 13.6, which was significantly higher than the norm in China. In their meta-analysis of relevant literature from 1994 to 2011, Whittemore et al. suggested that the prevalence of anxiety symptoms of parents of children with T1DM was 21% to 59%, and the detection rate of anxiety was high. Consequently, they recommended preventive measures. On the other hand, our conclusions were not consistent with Makara-Studzińska et al. [30], who used the Hospital Anxiety and Depression Scale (HADS) to investigate the anxiety in 120 mothers of children with T1DM. The results showed no significant difference in anxiety levels between the mothers of children with T1DM and healthy children. The possible reason for these discrepancies might be due to the use of HADS in the survey, which was inconsistent with our scale. Besides, the surveyed population only included mothers. The following are potential reasons explaining why the anxiety of the primary caregivers of T1DM children was at a high level. (1) T1DM is an incurable lifelong disease, and with the progress of the disease course, a variety of chronic complications tends to occur, increasing the heavy ideological burden of the caregivers [11]. (2) The management of T1DM is cumbersome, and it involves nutrition, exercise, medicines, monitoring, and extensive medical knowledge, which is difficult for some caregivers to deal with [12, 13]. (3) T1DM treatment requires expenses (lifelong medicine, frequent blood glucose monitoring test paper, complication examination, treatment, etc.), so the primary caregivers need to bear a greater economic burden [14]. All these factors can be associated with anxiety.
Our results revealed significant differences between the anxiety and non-anxiety groups among primary caregivers of T1DM children in terms of treatment method, Whether HbA1C to standard (≤7.0%), whether there was severe hypoglycemia in the last 1 year, and whether in adolescence, thus suggesting that these four factors might be affecting their anxiety. Furthermore, logistic analysis was conducted on the factors that could affect the anxiety of the primary caregivers. The results showed that adolescence, insulin pumps and HbA1C to standard (≤7.0%) were associated with anxiety, Adolescence and insulin pumps increase risk, HbA1C to standard (≤7.0%) reduce risk.
The possible reasons are as follows. (1) Adolescence is a transitional period in which a child develops into an adult. Children’s physical and cognitive development are not synchronized at this stage, and children tend to pay much more attention to their abilities. On the one hand, they desire their independence, but illness makes them dependent on medical care and caregivers, thus making the antagonism and rebellion more evident in adolescence. Related studies have proved that adolescence is a high-risk period for psychological and behavioral problems in T1DM children [18, 33]. Besides, the secretion of gonadotropin-releasing hormone and corticotropin-releasing hormone in the hypothalamus increase after adolescence, resulting in insulin resistance and increasing the difficulty in blood glucose control [34]. Previous studies showed that among children <18 years of age, blood glucose control was the best in pre-school age children and the worst in adolescence [35]. The difficulty of adolescent children’s reverse psychology and blood sugar control makes the primary caregivers of T1DM children more prone to anxiety. (2) An insulin pump is more in line with the physiological pattern of insulin treatment, as it can better control blood glucose and effectively avoid hypoglycemia [36]. Still, an insulin pump is also an expensive medical device, with a price ranging from 20,000 to 70,000 CNY. The one-time use of insulin pump injection components costs about 500 CNY per month, which is higher than the cost of multiple daily insulin injections. Therefore, insulin pump treatment puts more economic pressure on caregivers. An insulin pump is an artificial intelligence device with higher requirements on education and nursing level from primary caregivers [12, 13, 37]. The application of insulin pumps requires a higher economic and medical-related ability from primary caregivers. In clinic, we found that the primary caregivers who treated T1DM children with insulin pumps often had higher expectations of blood glucose control, which imminently increases psychological pressure. Economic pressure, educational requirements, and high expectations are probably associated with anxiety among primary caregivers of T1DM children. On the other hand, there might be a bias because primary caregivers who were originally anxious about the risk of hypoglycemia and future complications choose the pump treatment. Nevertheless, continuous glucose measurement devices are also expensive and require knowledge and skills, but they were not associated with anxiety. A possibility is that glycemia does not need to be measured multiple times a day when control is good. (3) Previous studies showed that HbA1C was an independent risk factor for coronary artery disease and associated with significantly increased risks of diabetic peripheral neuropathy among diabetic [38, 39]. HbA1C to standard can reduce the occurrence of complications and can reduce primary caregivers worry about the physical status of children with T1DM. So HbA1C to standard can reduce anxiety among the primary caregivers of children with T1DM.
This study was cross-sectional, which cannot determine causality. These points will be examined in future studies.
This study has some limitations. First, this was a single-center study with relatively low representativeness. Multicenter data from other provinces and cities need to be collected for further analysis. Second, the influence of anxiety of the primary caregivers on blood glucose control and the growth and development of children was further discussed. Third, no detailed analysis was made on the occurrence of anxiety among the primary caregivers at different stages of the disease course, which will be a direction of our future research. Fourth, the COVID-19 quarantine policies in China required that only one caregiver could accompany each patient, and both parents could not be evaluated. In addition, the COVID-19 pandemic was an important factor that might have increased the general anxiety level of the caregivers [40, 41]. On the other hand, the quarantine policies were the same for all citizens.
In conclusion, the primary caregivers of T1DM children had high anxiety levels. There were significant differences between the anxiety and non-anxiety groups in treatment method, HbA1C to standard (≤7.0%), whether there was severe hypoglycemia in the last 1 year, and whether in adolescence, among which adolescence, insulin pump treatment increase anxiety. Pediatric endocrine care should help T1DM children manage their disease and pay attention to the anxiety of their primary caregivers, especially those whose children are in adolescence and wear insulin pumps. More support should be given to primary caregivers with anxiety tendencies to reduce the occurrence of anxiety.
This work has been carried out in accordance with the Declaration of Helsinki (2000) of the World Medical Association. This study was approved by the Ethics Committee of Henan Children’s Hospital (2020-NMF-016), and all participants provided written informed consent.
Consent for publicationNot applicable.
Availability of data and materialsThe datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Competing interestsThe authors declare that they have no competing interests.
FundingThis study was supported by the Medical Science and Technology Project of Henan Province (2018020648) and Key Science and Technology Project of Henan Province (142102310139).
Authors’ contributionsAuthor contribution statement: Fang Liu: study design, data collection, data sorting, statistical analysis, manuscript writing; Qiong Chen, Mengmeng Du, Yan Cui, Ai Huang, Yangshiyu Li: data collection, data sorting, and statistical analysis; Haiyan Wei, Bingyan Cao: study design, research guidance, manuscript revision, financial support.
AcknowledgmentWe wish to thank all the T1DM children and their primary caregivers who participated in this study.
