Introduction

Type-1 diabetes mellitus (T1DM) is an endocrine-metabolic disturbance that occurs as a result of the devastation of the pancreatic beta cells under autoimmune infirmity and genetic influence [1]. T1DM is mainly a disease of childhood and adolescence characterized by insufficient insulin production and subsequent increase of the blood glucose level (i.e., hyperglycaemia) [2, 3] . Despite the global nature of the disease, its incidence shows geographical heterogeneity. For instance, a very low annual incidence has been reported in China and Venezuela (0.1 per 100,000 individuals) while in Finland, the incidence is high (40.9 per 100,000) [4]. In Egypt, the number of new cases rises progressively; in a retrospective survey to figure out the prevalence of T1DM among children and adolescents, it was found unremitting increases in the disease prevalence over the period from 1994 to 2011 to reach 26.8 per 100,000 [5]. The oral health status of diabetic children is the pivot of several investigations. Oral complications are common among adolescents with T1DM, especially those of poor metabolic disease. Periodontal diseases and opportunistic candidal infection are well-established sequelae of diabetes. A controversial data correlate dental caries with diabetes; high caries may be related to reduce salivary flow [6,7,8,9]. In contrast, other studies have not confirmed this relationship [2, 10].

Oral health is an integral part of the multi-dimensional aspects of an individual’s general quality of life perception. Oral health has an influence on physical, psychological, social and emotional life aspects [11]. One of the tools designed by Jokovic et al. to measure oral health-related quality of life (OHRQoL) in children is child perception questionnaire (CPQ) for age groups 8 to 10 years (CPQ8–10) and 11 to 14 years (CPQ11–14) [12].

Several epidemiological studies have evaluated the association between diabetes and quality of life. However, most of these investigations have focused on adults with type-2 diabetes. The main concern of these studies was the general health-related quality of life (HRQoL). In addition, most of these investigations have been conducted in developed countries and a little was known about OHRQoL in children and early adolescents with T1DM in developing countries.

In Egypt, the number of new cases suffering from T1DM rises progressively and the available data concerning children and early adolescent’s OHRQoL and OHS among Egyptian children and early adolescents with T1DM are still obscured. Therefore, the current study was conducted on a group of Egyptian children and early adolescents with T1DM aged from 8 to 14 years to (1) evaluate their OHRQoL and the impact of individual, environmental, oral health care and biological independent predictors and (2) assess their oral health status (OHS) in terms of oral hygiene, caries experience, untreated carious cavities and gingival condition.

Materials and methods

Setting, design and sample size determination

The study was conducted on diabetic children, who attended the Endocrinology Outpatient Clinic, Paediatric Department, Faculty of Medicine and Paediatric Dentistry Department, Faculty of Dentistry, Minia University during the period from February 2018 to January 2019.

Based on the estimated standard deviation (15.5) of the OHRQoL scales obtained from a pilot study included 70 diabetic participants (35 children and 35 teenagers), 0.05 degree of precision, a power of 0.8 and 5% significant level; 201 diabetic participants were enrolled in this cross-sectional investigation. An additional 21 children (10%) were included to compensate the non-response cases. The total number of diabetic participants was 222 and, for comparison, another 222 healthy children were recruited. The two groups to be matched, the children in the control group were selected randomly from the same schools, age and gender of the diabetic children.

Eligibility criteria

Inclusion criteria

The children included in the current study must have the following criteria:

  1. 1.

    Aged from 8 to 14 years

  2. 2.

    Medical reports revealed T1DM exclusively with a minimum of 2 years of diagnosis [13]

  3. 3.

    Only caries experience and gingival status were selected to represent the clinical variables that may mediate the children’s OHRQoL

  4. 4.

    No emergency dental recall in the last 3 months [14]

Exclusion criteria

Children with the following condition have been excluded:

  1. 1.

    Orthodontic treatment or malocclusion

Systemic, psychological or intellectual disabilities

Allocation

Eligible participants in both groups were selected using a computer-generated simple randomisation. Then, they were assigned into four groups: (i) case group (8- to 10-year-old children with T1DM), (ii) control group (8 to 10-year-old children without T1DM) (n = 125 children per each group), (iii) case group (11 to 14-year-old early adolescents with T1DM) and finally, (iv) control group (11 to 14-year-old early adolescents without T1DM) (n = 97 early adolescents per each group).

Study measuring tools and variables

The variables adopted in this study were classified into five levels based on previously suggested variables by Sischo and Broder [15]. The first level considered the following individual characteristics: (i) demographic data (e.g., gender) and (ii) the metabolic disease status evaluated using the glycated haemoglobin level (HbA1c) adjusted as less than or equalled 8% and over 8% [16]. The second level included the environmental predictors in terms of socioeconomic status (SES) that incorporated

  1. 1.

    Mother and father’s levels of education, which were categorized into four classes: “greater than secondary, secondary, less than secondary and illiterate” [17]

  2. 2.

    Household expenditures per person recorded in the local currency (Egyptian LE) per month then divided by 30 days. The cut-off point of poverty per day in Egypt was US$1.99 [17, 18].

  3. 3.

    Dental service utility, represented with a question about the regular annual dental visit “yes” or “no” response.

The third level scrutinized the personal oral health care, including the frequency of tooth brushing and mouthwash that assessed through three responses: “none, three times or less/week, once/day and twice/day”. For dichotomization, none or three times or less/week responses were considered as “irregular” frequency use and once/day and twice/day were considered as “regular” frequency use. The fourth level considered the biological factors that the oral health status (OHS) in terms of (i) caries experience measured with decayed, missing and filled teeth index (DMFT) of permanent teeth for caries experience and decayed teeth index (DT) for untreated carious cavities. Both indices were addressed as “0” or “≥ 1”. (ii) Oral hygiene and gingival condition were appraised using the Plaque index (PI) and Gingival index (GI), respectively. PI scores classified excellent/good oral hygiene (0–0.9), fair oral hygiene (1–1.9) and poor oral hygiene (2–3). GI scores categorised as no/mild gingivitis (0–1), moderate gingivitis (1.1–2) and severe gingivitis (2.1–3) [19]. To assess the OHRQoL, a face-to-face interview was using a validated Arabic version of CPQ8–10 and CPQ11–14 short-form questionnaires. Responses categorized on a 5-point Likert scale: 0 never, “1” once or twice, “2” sometimes, “3” often and “4” every day or almost every day [20,21,22] (Appendix 1).

Data collection and calibration

Before launching the study, two dentists with at least 2 years of residency at the Paediatric and Dental Public Health Department, Faculty of Dentistry, Minia University, were trained for 1 week. After the training period, all the investigators involved in the study and their recorded DMFT, PI examined 47 children and GI scores examined for reliability. Dental caries examination performed by a visual-tactile method using a dental mirror and WHO probe plus previous tooth brushing and air-drying for 5 s per each dental surface under artificial light [23, 24]. The gingival condition was evaluated using the gingival index (GI), and the criteria of Loe and Silness were adopted to calculate the GI scores [25].

Statistical methods

Statistical Package for the Social Sciences (SPSS) version 20 was used for data entry and analysis. Descriptive statistics included frequency tables, mean and standard deviation (SD), median and interquartile range (IQR) of CPQ11–14 different domains. Both Mann-Whitney U binary non-normally distributed data. To inspect the relationship between metabolic disease control and study different OHS representatives, Pearson’s correlations have been used.

Log-linear Poisson model regression analysis was performed to determine associations between the OHRQoL and independent predictors. Statistical models in the current study were released according to a hierarchical strategy of determinant factors. Predictors were categorized into four models; “Model 1” included the individual characteristics, “Model 2” incorporated model 1 plus environmental factors, “Model 3” contained Model 2 plus the oral health care predictors and Model 4 implicated model 4 plus the OHS variables. At each level and after bivariate analysis, predictors with a level of significantly lower than 0.2 (p ˂ 0.2) were included in the subsequent model until constructing the final model. For bivariate and multivariate statistical analysis, independent variables were dichotomized. The cut-off point of the level of significance was specified at less than 5% (p ˃ 0.05) and 95% confidence interval (95% CI).

Results

Out of the examined 579 children and early adolescents, 444 participants were selected. The response rate was high 100% and 98% in the case and control groups The inter-examiner reliability of DMFT and DT scores Kappa coefficients (κ) was 0.93, and for PI and GI, the degree of agreement was 0.87 and 0.89 respectively. Cronbach’s alpha of the CPQ of different domains in the children group with T1DM ranged from 0.76 to 0.88 and from 0.78 to 0.91 for the early adolescent group.

Based on the cut-off point of HbA1c, the frequency of poorly controlled children with T1DM was 117 (93.6%). In the early adolescent group, the frequency of both uncontrolled and controlled diabetic status was 74 (76.3) and 23 (23.7) respectively. The prevalence of sever gingivitis was predominant among early adolescents The prevalence of dental caries (DT ≥ 1) in the children and early adolescents with T1DM was 49.6% and 79.4% group with diabetes (75.3%). On the other hand, poor oral hygiene was prevalent in the children group with T1DM. The other baseline characteristics and objective measures are illustrated in Table 1.

Table 1 Baseline characteristics of the diabetic group and the non-diabetic group
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The data in Table 2 showed a distinct statistically significant difference between the study and control groups concerning the OHS. Children and early adolescents with T1DM showed a higher average of untreated carious cavity scores compared to their peers without T1DM. Despite that poor oral hygiene was obvious in all groups, the average PI scores in the two case groups were statistically significantly higher than those recorded in the control groups (p ˂ 0.01). The worse gingival index (GI) mean and median scores were recorded among early adolescents with T1DM [mean (SD) = 2.24 ± 0.61; median (IQR) = 2.3(1)] indicating severe gingivitis. Other groups revealed moderate gingival inflammation. The average and median scores of HbA1c in the early adolescents with T1DM were 11.85 ± 0.65 and 10.8(2) respectively which are higher than the records of children with diabetes [mean (SD) = 8.68 ± 1.37, median (IQR) = 8.8(1)] (not shown in the table). A statistically significant difference in the overall CPQ mean and median scores between the participants with and without T1DM in the two groups have been disclosed (p ˂ 0.01). The social well-being of CPQ domains was a prominent concern that negatively affected children and early adolescents’ life aspects.

Table 2 Median and interquartile range of child perception questionnaire (CPQ) domains of the diabetic and the non-diabetic groups
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There is strong correlation between OHRQoL and the level of HbA1c in the two diabetic groups (r = 0.69 for children group and 0.74 for the early adolescent group). (Figure 1). Moderate correlations between HbA1c of children group and DMFT, DT, GI and PI scores have been recorded as follows: [r = 0.18 (p ˂ 0.05), 0.59 (p ˂ 0.01), 0 .31 (p ˂ 0.01) and 0.44 (p ˂ 0.01)] respectively. For the early adolescent group, there is strong highly significant correlation between HbA1c PI and GI scores (r = 0.66 and 0.61) respectively and a moderate correlation with DT (r = 0.48) and DMFT scores (r = 0.42) with a high level of significance (p ˂ 0.01).

Fig. 1
figure 1

Pearson’s correlation (r) between OHQoL and glycated haemoglobin of children group a r = 0.69 and early adolescent group b r = 0.74

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The association between different study variables and the OHRQoL is declared in Tables 3 and 4. There was no statistically significant difference in the overall CPQ scores between males and females in all groups. In addition, the father’s level of education was not statistically significantly associated with OHRQoL and this was in contrast with the maternal level of education, which was statistically associated with the OHRQoL average and median scores. The gingival condition had no statistically significant impact on the children with T1DM (p > 0.05) while its impact was evident among early adolescents with T1DM (p ˂ 0.01). High dental plaque accumulation was statistically significantly associated with high scores of OHRQoL in all groups except for children without T1DM.

Table 3 Mean rank of the HbA1c in relation to the oral condition and DMFT, PI, GI scores and the CPQ domains scores of the study groups
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Table 4 Beta coefficient of the OHRQoL, caries experience and gingival status of diabetic and non-diabetic children in relation to the socio-demographic variable, economic factor, dental care, DMFT, GI and PI scores
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The final model of log-linear Poisson regression analysis demonstrated that the odds ratio (OR) of poor OHRQoL among children and early adolescents with poor metabolic control was 1.30 [95% CI 1.18–1.47] and 1.22 [95% CI 1.11–1.38] times more than those with good metabolic control do. The mother’s education had a statistically significant influence on the OHRQoL of both groups with diabetes, while the father’s education level does not seem to catch such effect. In the children group with diabetes, the OR of caries experience showed no statistically significant effect on the OHRQoL and this was contrary to the untreated cavities and gingival condition that revealed a statistically significant influence on the CPQ overall score. Concerning the early adolescents with T1DM, the OR of OHRQoL was 1.18 [95% CI 1.11–1.29] times among the participants with poor gingival and oral hygiene in comparison with those with good gingival and plaque status. In addition, the OR of OHRQoL among early adolescents with untreated cavities was 1.17 [95% CI 1.10–1.26] when compared to those without carious lesions (Table 4).

Discussion

The current study was designed as a case-control study that aimed mainly to assess the OHS among a group of children and early adolescents with T1DM and its impact on their OHRQoL. A face-to-face interview has been chosen to perform this study because of the guarantee of obtaining a high quality and more accurate data [26].

Although there were several researches concerned with DM and its influence on the quality of life, it was difficult to implement a direct comparison between the findings of the current study and previously published findings. This might be attributed to a number of reasons. For instance, (i) the methodology and design variability (i.e. the use of different tool for measuring OHRQoL, number of recruiting participants and their age groups) and (ii) the difference in participants’ baseline characteristics as well as the divergent socioeconomic backgrounds. However, it was useful to highlight some of these findings.

The findings of the present study highlighted that emotional difficulties were the apparent concern among children and early adolescents with T1DM. This was in agreement with outcomes of Roa et al. who declared a negative impact of DM on the emotional and psychosocial aspects [27]. This might be explained through linking the social well-being to social-environmental determinants such as socioeconomic status and the level of education of early adolescents’ parents/caregivers that diminish the participant’s self-management of the disease [28]. Low family income and parental education level also constrained dental services utility and oral hygiene measures [29]. This was in line with the results of the current study, which elucidated the correlation between socioeconomic status and untreated carious lesions and its subsequent inferior influence on OHRQoL. Psychological difficulties might be aroused from the lack of awareness about the importance of family support. This explanation is supported by Frank’s claim that psychological issues are related to the care of adolescents with T1DM, as well as Noueiri and Nassif, who declared that the negative impact of psychological changes reaches the peak in the adolescence stage [30, 31]. The study findings emphasized the negative impact of poor metabolic control of T1DM on the OHRQoL. Psychological make-up plays a key role in metabolic disease control in terms of lack of adherence to insulin therapy and diminished efficient self-management behaviour [32].

The current study declared the negative impact of poor metabolic glycated control on the OHRQoL.

This influence might be correlated with the poor OHS recorded by the children and early adolescents with T1DM. Concerning dental caries, the results revealed a significant difference between the diabetic and non-diabetic participants of both age groups. Several former studies supported our point of view [33, 34], while other published articles denied the association between diabetes and dental caries in children and early adolescents [35, 36]. This heterogeneity might be related to the variation of caries prevalence among the studied population, different sample sizes or the selected HbA1c cut-off points may play a role in such differences. In the present study, the high caries experience could be attributed to the following: (i) poor oral hygiene in commitment with an obvious shortage in oral health care especially among children with T1DM and (ii) poor glycemic control might contribute in diminishing the salivary flow and buffer capacity and subsequent increase of the cariogenic bacteria such as streptococci and lactobacilli [37]. Moreover, high levels of Hba1c might be associated with poor dietary habits and higher intake of saturated fat [38].

The outcomes of the present study showed a significant association between dental plaque, gingival inflammation and the level of HbA1c. This was in agreement with the data published by Al-Khabbaz et al. who demonstrated a statistically significant difference in the GI and PI scores between the diabetic children aged 4 to 14 years and the non-diabetics [39]. Furthermore, the number of gingival bleeding sites as an indicator of gingival status was found to be statistically significant in children with diabetes in previous investigations [40, 41]. These observations could be due to the poor metabolic control that prompted the accumulation of dental biofilm. This augmented the host defence mechanism especially when accompanied with improper oral hygiene [42].

The pervasiveness of poor OHRQoL was obvious among not only the T1DM participants, but also non-diabetic children and teenagers that suffered from the predatory impact of low SES, potentially conjugated with limited access to care. Furthermore, low SES might not force the parents/caregivers to deem oral health care a major concern among their vantages. Parent’s education had a positive effect on the OHRQoL. Increasing the level of education might boost the awareness, attitude and practice toward enhancing their children’s oral health care. This was in line with the findings of former published findings [43, 44]. The frequency of dental visit and gender showed no significant impact on the OHRQoL which was compatible with a previous article finding [45].

Study strengths and limitations

Some limitations of the current study warrant consideration. Firstly, the whole participants were recruited from a public health centre, which is mainly the destination of low SES families and might influence the generalization of the findings. Secondly, depending on visual-tactile method only to calculate the DMFT scores without the aid of bitewing radiographs might underestimate the findings of caries background. Finally, recall bias might be encountered in the children and early adolescents’ responses.

However, the present study has several strong points, which could be concluded in the following aspects: (i) the high reliability, which is important for the internal validity of the study. (ii) To improve the data accuracy, a face-to-face interview was considered which aided in expressing and recording the true feelings of the participants rather than depending on the self-reported questionnaire. This method guaranteed that the extracted data were accurate, and this might explain the high reliability of variable scales. (iii) Up to the data, it is a premier studies that assessed the quality of life of children with T1DM in Egypt at these age groups.

Conclusions

In sum, the overall self-reported OHRQL appears to be adversely affected by the presence of diabetes especially among children and early adolescents with poor metabolic control. Children and early adolescents with T1DM showed a higher prevalence of caries experience, untreated carious cavities and gingival inflammation in comparison to their counterparts without diabetes. SES and oral health care demonstrates a significant impact on the OHRQoL; however, the effect was obvious in the diabetic and non-diabetic groups. This study highlighted the urgent need for improving the oral health status of early adolescents with T1DM and enforcing the role of preventive oral hygiene measures.