Assessment of Dental Status and Oral Health Status in Children with Congenital Heart Diseases

Department of Pedodontics and Preventive Dentistry, Santosh Dental College and Hospital, Ghaziabad, UP Director, Smileoracles Dental and Allied Services, LLP, New Delhi Division of Pediatric Cardiology, Postgraduate of Institute of Medical Education and Research, Dr. RML Hospital, New Delhi Department of Biostatistics, All India Institute of Medical Sciences, New Delhi Department of Cardiothoracic and Vascular Surgery, All India Institute of Medical Sciences, New Delhi


Introduction
The prevalence of caries in children with congenital heart disease (CHD) in India, where children are not offered organised dental care from an early age is unknown. Developmental enamel defects, inadequate oral hygiene and unawareness of dental diseases among parents make them prone for dental caries. Bacteraemia induced by dental caries and dental procedures predispose these children to life threatening infective endocarditis [1,2]. Various haematological, respiratory, and immunological morbidities associated with CHD and drug interactions associated with cardiac medications should be considered while managing the dental pathology [1] Moreover, the affected children have a reduced tolerance to stress induced by dental treatment [3]. Therefore early/preventive dental care of children with CHD is vital. The incidence of CHD across the world is approximately 8-10 cases per 1000 live births [4,5]. The prevalence of CHD in India is 19.2 per 1000 individuals and CHD alone accounts for 10% of the total infant mortality in India. According to the 2001 census data, there are 28 million live births per year in India. Going by the incidence of 8/1000 live births, 60,000-90,000 in a total of 1,80,000 children have CHD in India. 4 With advances in medical and surgical management, most of the children with CHD survive into adulthood resulting in the introduction of a new group of patients in dentistry. Despite advances in cardiac management, there is a lack of information regarding the dental health and treatment requirements of these patients [4,5]. With this background, we conducted this study with the primary objective to compare the prevalence of dental caries and dmft/DMFT scores amongst children with CHD and healthy controls. The secondary objective was to investigate the dental health practices and the risk factors for dental caries in the children with CHD.

Methods
This study conforms to the principles outlined in the declaration of Helsinki and approved by the Institutional Ethics Committee. The study included surviving children with CHD aged between 2 to 5 and 12 to 15 years. These two age groups were selected as per the recommendation of WHO Oral Health Survey 2013 that laid down 5 years as the index age group for primary dentition and 12 years as the index age for permanent dentition [6]. Children aged between 6 and 11 years (the mixed dentition group), children with concomitant severe congenital non-cardiac diseases like congenital nephrotic syndrome, exomphalos, tracheoesophageal atresia, tracheoesophageal fistula, anal atresia, Hirschsprung's disease, thalassemia, vonWillebrand disease, idiopathic thrombocytopenic purpura, children with learning difficulties and cerebral palsy, and those who did not have the consent to participate were excluded from the study.
The present study has a descriptive crosssectional design. The sample size was calculated to estimate the true prevalence of the disease with 95% confidence level, α=0.05, Zα=1.96 (value of Z from probability tables), prevalence= 20% (calculated from the pilot study), and precision of the estimate (d)=10 (taking relative precision of 20% Based on age at presentation, the patients were allocated to two groups: Group I: primary dentition (age 2-5 years; CHD, n=150; control, n=423) and Group II: permanent dentition (age 12-15 years; CHD, n=86; control, n=528). The children with CHD had a migratory background and hence were further subdivided according to the location into urban, peri-urban and rural.

Results
The distribution of the samples in the CHD group according to age, gender, and geographical location is depicted in Table E1. Patients' age at evaluation ranged from 2 to 5 years (mean 3.5±1.1, median 4 years) among those with primary dentition (group I) and 12 to 15 years (mean 13.3±1.05, median 13.5 years) among those with permanent dentition (group II). Both the groups had male preponderance (group I: 75.3% and group II: 81.4%). The mean dmft±SD and mean DMFT±SD scores for dental caries were higher in the study group than in the control (group I: study vs. control: mean dmft±SD=2.42±3.81 vs. 0.009±0.13, p<0.001; group II: study vs. control: mean DMFT±SD=2.15±3.37 vs. 0.14±0.09, p<0.001) ( Table E2). The mean dmft±SD scores were similar in both genders in the primary dentition group. The mean DMFT±SD scores were significantly higher among males with CHD (mean DMFT±SD=1.06±2.04 vs. 0.13±0.8, p=0.01) (Tables E3A, E3B).
In the permanent dentition group, the mean DMFT±SD score was higher in children with Page: 45 www.raftpubs.com CHD coming from rural areas than in those from urban and peri-urban areas (p=0.001). However, such difference was absent in the primary dentition group (p=0.2) ( Table E3C). The primary dentition group did not exhibit any significant difference between cyanotic and acyanotic congenital heart disease for dmft scores. In the permanent dentition group, cyanotic patients had a higher DMFT±SD than did acyanotic patients (mean DMFT±SD=3.04±4.2 vs 1.12±1.5, p=0.006) ( Table E4). The dmft/DMFT scores were significantly higher in children who perceived their health of teeth as poor, followed by average and good in both the age groups (Table  E5A). The dmft scores were significantly higher in children who perceived their health of gums as poor, followed by average and good in group I (Table E5B). The gum health did not affect the DMFT scores in group II according to the perceived health of gums (Table E5B). In group I, dmft indices were significantly higher in children visiting the dentist than in children who never visited the dentist (Table E5C). There was no significant difference in the dental caries index among children of both groups according to the frequency of cleaning teeth and usage of toothbrush and toothpaste (Table E5D, E5E). A majority of subjects brushed their teeth once a day. In group I, dmft scores were significantly higher in children frequently consuming biscuits and confectionary (2.10 ± 3.33; p=0.01) and milk with sugar (2.14 ± 3.37; p=0.008) (Table E6). In group II, DMFT scores were significantly higher in children frequently consuming tea with sugar (1.06 ± 1.72; p<0.001). There was no statistically significant difference in the dental caries index of children with CHD in both the groups according to the parents' level of education (Table E7). In group I, dmft scores were significantly higher in children who missed school due to toothache. The mean dmft scores were 7.21 ± 5.03 (n=24), (missed school) versus 1.52 ± 2.74 (n=126), (did not miss school), (p<0.0001) (Table E8). Intervention urgency in children with CHD was grouped into four categories (Table E9). The majority of the children needed either preventive (n=81) or routine (n=55) treatment; only six children in group I needed urgent treatment. The mean dmft scores were significantly high in the children requiring routine (5.02 ± 3.44) or urgent (10.83 ± 7.49) treatment, compared to children requiring only preventive treatment (0.27±0.65). As the severity of caries increased, there was a greater need for routine or urgent treatment intervention in primary dentition (Table E9). All the children in group II required either preventive (n=37) or routine (n=49) treatment. The mean DMFT scores were significantly high in children requiring routine treatment (3.35 ± 3.98) compared to those requiring preventive treatment (0.54±1.10) in group II (Table E9).
In the present study, when bivariate logistic regression analysis was applied (Table E11, E12), the possibility of caries in permanent dentition was high in children with cyanotic CHD compared to acyanotic CHD (OR=3.46; 95% CI=1.24 -9.64). Cyanotic CHD was positively associated with caries experience in permanent dentition (p=0.01).

Assessment of Dental Status and Oral Health Status in Children with Congenital Heart Diseases JCSHD: June-2019: Page No: 42-58
Page: 46 www.raftpubs.com Table E1: Demographic details of the study group of patients with congenital heart diseases and the control group.
Hoffman and associates demonstrated that countries with high fertility rates tend to be those with lower per capita income and more births per unit of population [9]. They have a disproportionate number of children born with congenital heart disease; this imposes an added burden. Poverty compounded by limited education forms a high barrier to successful treatment of CHD [17]. With the advent of paediatric cardiac surgery in 1938 along with modern diagnostic tools; most of these children survive into adulthood [18]. However, the burden of a severe medical condition, multiple medications and long periods of hospitalisation Page: 53 www.raftpubs.com in these children lead to neglect of oral health and of its effect on their general health over time [1,7,19,20].
For both group of patients with primary and permanent dentition, the dental caries index scores were high in the study group compared to healthy control (Table E2). The results of the present study corroborate the findings of other studies [1,16,21,[23][24][25][26][27]. This could be due to decreased dental intervention in the cardiac group compared to the control group, high complexity of CHD disease and increased health demands made by their medical condition. Children who experience extensive decay in the primary dentition group are at risk for future proximal molar decay despite implementing preventive measures [21,22]. Our findings are at variance with Tasioula and associates who found that children with CHD had similar levels of dental disease compared to children without this congenital anomaly [7]. This could be attributed to the intervention in, and successful management of, these patients at an early age [7]. The results of our study were statistically significant for the CHD group in the permanent dentition group, with higher caries index in males than females (Table E3A,  E3B). This finding conforms with a study by Joshi and associates who found that overindulgence and frequent feeding of males over females prevail in India regardless of the socio-economic class [23]. In this study, mean DMFT score was high in permanent dentition in rural areas (Table E3C). This may be attributed to factors like family income, parental education, parents' dental knowledge, attitude and behaviour, the child's dietary and oral hygiene habits, and place of residence [24]. Further support regarding the positive correlation of dental caries with the above factors comes from studies conducted in Greece [25], Hong Kong [26] the UAE [27] and China [28]. Studies conducted on caries in rural areas of Uganda [29] and Southwestern China [30] showed that decayed teeth accounted for the greatest percentage of total dmft/ DMFT. Similar findings on caries experience were reported in rural areas of Maharashtra [31], Karnataka [32] and Punjab [24] in India. Although higher than the WHO target, there was no statistically significant difference between the cyanotic and acyanotic groups for dmft scores in the primary dentition group (Table E4). In the permanent dentition group, DMFT scores in the cyanotic group were significantly higher than in the acyanotic group. Berger and associates demonstrated that cyanotic children had more active carious teeth, received fewer reminders to brush from their mothers, had more cariogenic food at home, and lowest levels of dental treatment [15]. Seymour and associates also demonstrated that bleeding gums with anticoagulants and gingival hyperplasia due to calcium channel blockers compromised the oral health conditions in these children [33]. Furthermore, Stecksen-Blicks and associates showed the association of digoxin and dental caries in children with CHD because of its availability in sucrose-based suspension (Lanoxin) [20]. In addition, studies by Linda Rose [34] and Stecksen-Blicks [10] reported that diuretics increase the risk of caries and hyposalivation. Owing to the compounded chair-side risks of medical emergencies dental care is often of low priority in this group as in agreement with Franco and associates [8]. Thus, children with cyanotic heart disease are at increased risk of developing dental and gingival diseases.

Assessment of Dental Status and Oral Health Status in Children with Congenital Heart Diseases JCSHD: June-2019: Page No: 42-58
Page: 54 www.raftpubs.com The dmft/DMFT scores were significantly higher in children who perceived their health of teeth as poor in both the age groups (Table  E5A). Therefore, it appears that children with CHD were able to identify the problem and could be symptomatic due to the high caries tendency. This finding corresponds with Stecksen-Blicks, and was applicable to both the dentitions. However, their visit to a dentist was deferred until a caries problem was evident [20]. In the primary dentition group, dmft indices were significantly higher in children who perceived their health of gums as poor (Table E5B). This could be due to lack of supervised tooth-brushing and inability to take good oral care independently in children of this age group [8]. Primary teeth are also more predisposed to demineralization than mature permanent teeth due to the thinner and immature enamel, as stated by Franco and associates [8]. In the primary dentition group, dmft indices were significantly higher in children visiting the dentist compared to children who never visited the dentist (Table  E5C). Several children with CHD experience long hospital stays because of surgery or illness. Many of them never visit a dentist until a caries problem is evident [20]. Their burdens of financial and medical concerns make dental needs a lesser priority [2,16]. Page: 55 www.raftpubs.com In the present study, a majority of subjects brushed their teeth only once a day. There was no statistically significant difference in mean dmft/DMFT scores in primary and permanent dentition on intra-group comparison according to frequency of cleaning teeth (Table E5D). But the scores were higher than the WHO target. Lockhart and associates [35] recommended more attention to avoidance of dental disease in patients susceptible to endocarditis. Daily supervised tooth brushing has been shown to reduce dental caries in children [35]. In the primary dentition group the dmft scores amongst those who practiced tooth brushing were not significantly different from those who did not use a toothbrush (Table E5E). All the children in the permanent dentition group used a toothbrush and toothpaste for cleaning their teeth. However, the caries prevalence in both the study groups was above the WHO target (DMFT/dmft1.5) [6]. This showed the need for better oral hygiene practices to reduce caries experience. In our study, the mean dmft scores for children frequently consuming biscuits, confectionary and milk with sugar in the primary dentition group (>2.10) was higher than the WHO target [6]. The mean DMFT score in the permanent dentition group for children frequently consuming tea with sugar was 1.06 ± 1.72, which was within the WHO target (Table E6). This could be because biscuits, confectionary and milk with sugar are fermentable carbohydrates, whose frequent consumption may cause a fall in the pH leading to a constant acidic environment in the oral cavity. In a systematic review conducted in 2001 by Burt and colleagues, it was stated that sugar consumption in high frequency and amounts appear to be a risk factor for caries among some children, but not all [36]. Further research is needed to identify the factors that render some children more likely than others to develop caries in the presence of a high sugar diet. Studies have shown that parents of chronically sick children (like CHD) tend to overprotect and overindulge their child. Because of the reduced appetite of these children, parents often let their child eat and drink what they prefer (mostly sugar-containing beverages and cariogenic snacks), whenever they want (between main meals, at night), putting oral health at risk [23]. Also, children with CHD often need dietary modifications which may have damaging effects on their oral health. In the present study, there was no statistically significant difference in the mean dmft/DMFT scores of children with CHD in both the groups according to the parents' level of education (Table E7). Rai and associates stated that parents' awareness of the importance of maintaining good oral hygiene was very poor in India [9]. da Fonseca and associates reported that one-fifth of the parents of children with CHD did not know that oral health was important for their children's heart [37]. In the primary dentition group, the dmft indices were significantly higher in children who missed school due to toothache (Table E8). Jackson and associates have also shown a positive association between irregularity in school and dental problems [38]. The prevailing cardiac condition together with poor oral condition compounded the difficulties of the child and affected their regular attendance and education.

Assessment of Dental Status and Oral Health Status in Children with Congenital Heart Diseases
In the present study, the majority of the children needed either preventive or routine treatment; only six children in the primary dentition group needed urgent treatment. The mean dmft scores were significantly high in the children needing routine or urgent treatment than in children needing only preventive treatment (Table E9). As the severity of caries increased, there was a greater need for routine or urgent treatment intervention. This concurs with a study by Franco and associates [8]. Among the children with CHD, the need for routine treatment intervention was significantly higher in the cyanotic group compared to the acyanotic group (Table E10). When bivariate logistic regression analysis was applied (Table E11, E12); the possibility of caries in permanent dentition was 3.46 times more in children with cyanotic CHD than in acyanotic CHD (Odds ratio 3.46, 95% CI: 1.24-9.64, p=0.01). This was in concurrence with Stecksen-Blicks and Page: 56 www.raftpubs.com associates [20]. In the present study over 68% of the cyanotic CHD children required some type of dental treatment.
Congenital heart diseases-a potential risk factor for poor oral health or vice versa?
There have been several studies in the literature addressing poor oral health and its association with infective endocarditis in patients with CHD. However, the dynamicity of their interrelation has been inadequately explored. Ironically, CHD by itself could be a cause for the manifestation of the oral disease as stated by various authors. Cyanotic heart disease leads to altered structure of enamel and dentin with a significantly decreased calcium and phosphorus content in the saliva [39]. This is attributed to altered haemodynamics, chronic malnutrition, medication and hypoxia. Furthermore, Hansson and associates found cariogenic microflora like mutans streptococci at higher levels in CHD than case matched controls in infants at 12 months of age [34,40]. In addition, oral conditions like stomatitis, cyanotic oral mucous membrane, gingiva and tongue together with chronic malnutrition predispose these children to a higher incidence of enamel hypoplasia and periodontal disease [3].

Study Limitations
In this study, the control group was taken from school health surveys. We could take the control group from non-cardiac healthy patients reporting to the respective hospitals.

Conclusions
We conclude that children with CHD have poor oral health, and are prone to dental caries, compared to healthy children. Cyanotic heart disease patients have a higher caries experience than acyanotic patients. These patients should be given more attention due to their susceptibility to infective endocarditis.
Mothers, being the primary caregivers, should be aware about oral health care and nutritional needs of children with complex CHD. Hence, their education level has a close association with their child's well-being. Children with complex CHD often miss school due to toothache and debilitated health conditions. Lactose in milk together with sucrose in sugar and frequent food intake are contributory to the caries formation in the primary dentition group. Dental care is often a low priority in children with CHD, and is addressed only on occurrence of a problem. Closer collaboration amongst all medical professionals including cardiologists, dentists and nutritionists is needed in order to identify the children at high-risk and provide preventive oral care, awareness of oral hygiene, diet, and the benefits of fluoride supplements. Children with CHD should have their first dental check-up as the first tooth erupts, with follow up every 6 months. Dental surgeons should be appointed in Primary Health Centres (PHCs) to provide oral care in Rural India.