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Dental Caries, Oral Hygiene, and Oral Clearance in Children with Craniofacial DisordersDental Caries Research Group, Guy’s, King’s and St Thomas’ Dental Institute, Caldecot Road, Denmark Hill, London, England. SE5 9RW; Correspondence: * corresponding author, david.beighton{at}kcl.ac.uk
The reason that children with cleft palates tend to have a greater prevalence of tooth decay than normal children is unclear. We hypothesized that children with cleft palates would have increased oral clearance times for foods and, consequently, higher levels of caries and caries-associated micro-organisms than control children. Children aged 6–16 yrs, with (n = 81) or without (n = 61) cleft palates, were studied. Children with cleft palates had DMFT and dmft scores greater (p < 0.01) than those of the control group. The number of caries-associated organisms was greater in the saliva of the cleft palate children (all p < 0.001). The oral hygiene, plaque and gingival index scores were greater (p < 0.0001), oral clearance was longer (p < 0.01), and levels of sucrose and starch-derived saccharides higher (p < 0.01) in the cleft palate group. However, salivary concentrations of organic acids were lower in the children with craniofacial disorders, probably reflecting the altered physiology of the more mature dental biofilm. The longer oral clearance times of foods and the consequent generation of fermentable sugars from starches may contribute to the higher caries prevalence observed in children with cleft palates.
Key Words: cleft palate • plaque • caries-associated micro-organisms • starch • oral clearance
Craniofacial disorders are a relatively common congenital malformation. Facial clefting constitutes approximately 65% of the anomalies affecting the head and neck (Owens et al., 1985). The prevalence of dental caries in children is generally in decline in the UK, although it remains high in certain groups, including children with cleft palates (Dahllöff et al., 1989; Bokhout et al., 1996a; Hewson et al., 2001; Bian et al., 2001). This trend of more caries in children with cleft palates may be related to their particular difficulties in maintaining good oral hygiene, since studies have shown that cleft palate patients have poorer oral hygiene and periodontal health than do control subjects (Brägger et al., 1985; Dahllöf et al., 1989). There has been no adequate hypothesis proposed to explain these findings, but it would be expected that these craniofacial disorders adversely affect the carriage of caries-associated bacteria. Oral levels of mutans streptococci and lactobacilli were determined in Dutch children with cleft lip and/or palate (Bokhart et al., 1996), and 50% were colonized with mutans streptococci and 16% with lactobacilli at rates significantly greater than those found in children with no clefting. Teeth adjacent to the cleft were most often affected by caries (Bokhout et al., 1997), while children with cleft palates who had been bottle-fed had higher caries scores than control, bottle-fed children (Lin and Tsai, 1999). These studies suggest that children with clefts retain food in their mouths for longer periods than control children. High-starch-containing foods remain longer on the teeth than high-sucrose- or low-starch-containing foods (Edgar et al., 1975; Linke and Birkenfeld, 1999). The retention of high-starch-containing foods may give rise to prolonged periods of acid production (Kashket et al., 1994, 1996), which may promote tooth decay. On the basis of these previous reports, we have tested the hypothesis that children with cleft palates have increased oral clearance times, which is reflected in increased salivary levels of starch-derived saccharides, higher levels of caries-associated micro-organisms, and more caries than found in control children.
Subjects Eighty-one children with cleft palates attending the Craniofacial Multidisciplinary Clinics in London and 61 control children without clefts attending a Dental Trauma Clinic for treatment of accidental damage to their teeth and gums were recruited. For both groups, the inclusion criteria were that they had to be aged between 6 and 16 yrs, were able to produce an unstimulated saliva sample, and were not under active care for caries. The exclusion criteria were that they had not used prescribed antibiotics within the preceding 4 wks or were unable to provide an oral rinse. Informed consent was obtained from the parent accompanying each child. He/she was provided with an information sheet, and written consent was obtained for the inclusion of all children. For each child, the relevant medical history, use of topical fluoride treatments, a two-day diary of cariogenic snack consumption, residence, and ethnicity were recorded. The study was given ethical approval by King’s HealthCare Trust Ethics Committee.
Clinical Examination
Saliva Collection and Microbial Analysis
Oral Clearance and Saliva Rinse Analysis To demonstrate that starch degradation occurred in the mouth within the timeframe of the oral clearance experiments, we crushed a biscuit, suspended it evenly in 2% (w/v) molten agar at a concentration of 10% (w/v) and, while it was still molten, placed it within a short piece of PVC tubing (1.5 cm x 6 mm i.d.). After setting, the agar extending beyond the ends of the tubing was cut flat. Individual pieces of tubing containing the agar were held in the subject’s mouth for pre-determined periods of 1, 5, or 15 min, the agar was extruded from the tubing, and one end approximately 1 mm thick was cut off by means of a sterile scalpel blade for analysis. The samples were weighed and stored frozen until analyzed. Six healthy adult subjects participated in this aspect of the study. The oral rinse samples were thawed and centrifuged (3000 g) for the removal of debris, including residual biscuit. The supernatant from each sample was split to allow for the separate analysis of the soluble saccharides and the major bacterial acid end-products. We heated the samples for carbohydrate analysis to 95°C for 5 min to inactivate bacterial and host enzymes and to kill any micro-organisms. The samples for organic acid analysis were diluted 1:5 (v/v) in potassium chromate solution in de-ionized water (25 mg/L) and passed through a washed C18 cartridge (Sep-Pak, 50 mg, Waters Ltd., Milford, MA, USA). The agar samples were thawed, 1 mL of de-ionized water was added to extract sugars, and the samples were heated to 95°C for 5 min prior to analysis. All carbohydrate and acid analyses were performed with the use of a HPLC system (Dionex Corporation, Sunnyvale, CA, USA). A PA1 column and PA1 guard column trap were used to separate the sugars, which were eluted, at a flow rate of 1 mL per min, with the use of 150 mM NaOH in a 0- to 300-mM sodium acetate gradient over 50 min and detected by pulsed amperometric detection (PAD). An ICE-AS6 column was used to separate the organic acids. They were eluted with 0.4 mM heptafluorobutryic acid (0.6 mL/min) and detected by conductivity, after the eluent had passed through a membrane suppresser (Dionex), which was continually regenerated with aqueous 5 mM tetrabutylammonium hydroxide flowing at 5 mL/min. Concentrations in saliva were expressed as µM for the organic acids and mM for the sugars, while in the agar plugs the sugar concentrations were expressed as nmoles per mg of plug.
Analysis of Data
Comparison of the Oral Health Status of Subjects The children in the cleft palate group consisted of 40 males and 41 females with a mean age of 11.3 yrs, while the control group consisted of 31 females and 30 males (p > 0.1) with a mean age of 10.5 yrs (Table 1  ; p > 0.05). There was no significant difference in the health status, place of residence, or ethnicity of the two groups of children. Fluoride rinses or drops were used by only 10 cleft palate patients but by none of the control subjects. There was no difference (p > 0.05) between the mean number [± SE] of snacks consumed by each group per day, being 2.01 ± 0.11 for the cleft palate children and 2.18 ± 0.16 for the control children.
The children with different types of clefting were not significantly different and were analyzed as a single group. The children with cleft palates had significantly greater dmft (p < 0.001) and DMFT (p < 0.001) scores than the control children (Table 1  ). The children with cleft palates had significantly poorer oral hygiene scores ( 2 = 48.58; p < 0.001), significantly greater plaque scores (2 = 63.44; p < 0.001), and significantly greater GI scores (2 = 57.31; p < 0.001) than the control children (Fig.).
Comparison of the Oral Microflora of Subjects The salivary levels of mutans streptococci, lactobacilli, and yeasts were significantly greater (p < 0.001) in the cleft palate children than in the control children (Table 1 ).
Salivary Concentrations of Organic Acids and Sugars
The rapidity of the depolymerization of the starches in the plugs is demonstrated by the changes in concentrations of the starch-derived sugars in the plugs (Table 3 ). The sucrose and fructose, derived from the biscuit, were rapidly metabolized so that after only 1 min these were reduced significantly (p < 0.01), by 84% and 73%, respectively, and continued to be reduced over time. The glucose concentration was initially reduced but was present at a higher concentration in the five-minute samples and was reduced to a lower-than-initial concentration in the 15-minute samples. The concentrations of maltose and maltotriose, in particular, increased significantly (p < 0.01) after 1 min, by 7.7- and 72.5-fold, respectively, and remained at these increased levels throughout the exposure period.
Children with cleft palates had greater mean caries scores (as dmft and DMFT) than did the control children, confirming the finding for most other populations of cleft palate patients in several different countries. The factors associated with the increased caries levels in children with cleft palates are not fully understood. Multi-regression and dichotomous analyses have previously identified the educational attainment level of the mother, poor oral hygiene, and bottle feeding practices as important determining factors for caries in this group of children (Bokhout et al., 1996a,b; Lin and Tsai, 1999; Bian et al., 2001; Turner et al., 2001). In the present study, we also found that the oral hygiene and plaque scores and gingival index were significantly higher in the children with cleft palates compared with those in control children, confirming these earlier observations. In this study, the cleft palate children had higher salivary levels of mutans streptococci, lactobacilli, and yeasts, which may be associated with their poorer oral hygiene or their higher level of caries. Poor oral hygiene is often associated with higher levels of caries-associated micro-organisms in other groups of patients, as was found here for the children with cleft palates. However, there were no significant differences in carriage of mutans streptococci between children with cleft palates and good oral hygiene and control children (Lucas et al., 2000). These observations underline the profound influence of oral health on the oral microflora. Here we also investigated the oral clearance of a simple biscuit by measuring soluble sugars derived from the biscuit in oral rinse samples taken 10 min after the subject ate the biscuit. We chose to sample the mouth 10 min after the subject ate the biscuit, since, in other studies, it has been shown that the majority of any food, including starch-containing foods, is cleared from the mouth at that time (Luke et al., 1999). We therefore expected that if a difference in oral clearance times of foods were to be evident, then it would be most apparent at that time. Using these parameters, we demonstrated that the oral clearance times of these sugars by the children with cleft palates were apparently greater than those of the control children. The longer clearance time was evident from the higher levels of sucrose, which cannot be generated de novo from the biscuit, in the rinses from the cleft palate children and the generation of saccharides, by the action of salivary amylase, from the starches present in the biscuit. The generation of these sugars confirmed the rapidity of starch degradation observed in vitro (Grenby and Mistry, 2000), and the speed with which sucrose and fructose were utilized by the oral microflora was evident from the analysis of the sugars present in the agar plugs. pH changes in plaque, which are more relevant to caries, were not measured. Instead, we determined the salivary organic acid concentrations generated by the fermentation of the sugars from the biscuits, mediated by the intra-oral microflora. While the residual sugar concentrations were higher in the saliva of the cleft palate children, the salivary concentrations of organic acids were lower in the children with cleft palates than in the control children. This relationship does not seem to be what one would expect. However, in a recent study, acid production in plaque following sucrose exposure was negatively related to plaque mass, so that acid production, as acid per mg wet weight of plaque, decreased with increasing plaque mass (Borgstrom et al., 2000), and this may reflect changes in biofilm physiology resulting from oral biofilm maturation (Socransky and Haffajee, 2002). Thus, it would be expected that acid production from the children with cleft palates, with poor oral hygiene, and with high plaque score would produce less acid. Although the acid concentrations were less than in the control children, the longer oral clearance times of foods, and increased time for the generation of acids, may contribute to the increased caries levels in the children with cleft palates. The increased oral clearance times of foods have been identified in elderly patients (Lundgren et al., 1997), in patients with myotonic dystrophy (Engvall and Birkhed, 1997), and in rheumatic patients with dry mouths (Risheim et al., 1992) as a factor significantly associated with high caries activity. Analysis of these data supports our hypothesis and confirms the previous reports of significantly greater levels of caries in children with cleft palates. This was associated with poorer oral hygiene and higher levels of caries-associated microflora. The other critical finding presented here was that children with cleft palates had a significantly longer oral clearance time for a starch-containing biscuit, which would be expected to have deleterious effects on the dentition. Caries prevention in this group of children should therefore underline the need for good oral hygiene and the use of a fluoride-containing toothpaste. Additionally, these patients should be advised on the clinical consequences inherent in the longer oral clearance times of foods and should be advised of simple methods to reduce levels of residual foods following meals, especially snacks.
This project was supported by King’s College London. Received for publication January 6, 2003. Revision received October 16, 2003. Accepted for publication December 3, 2003.
Journal of Dental Research, Vol. 83, No. 2,
175-179 (2004)
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ABSTRACT
INTRODUCTION