ORIGINALAlaki ARTICLE et al
The Effects of Asthma and Asthma Medication on Dental Caries and Salivary Characteristics in Children Sumer Madani Alakia/Eman Anwar Al Ashiryb/Niveen Samir Bakryc/Khlood Khaled Baghlafd/Sarah Mustafa Baghere Purpose: To investigate the prevalence and severity of dental caries in children with a history of asthma in addition to their salivary characteristics, flow rate and buffering capacity, as well as the salivary level of Mutans streptococci (MS) and lactobacilli present. Materials and Methods: The study sample was composed of 30 cases and 30 controls with an age range from 5 to 13 years. The cases involved children with a past history of asthma, while the controls were medically fit children. The study was conducted from 2010 to 2011 and patients were randomly selected through the electronic filing system at King Abdul-Aziz University Hospital (R4 system), Jeddah, Saudi Arabia. Interviews and questionnaires were completed by the parents of the children involved and dental examinations were performed. Stimulated salivary samples were collected to determine the salivary flow rate, buffering capacity and salivary levels of MS and lactobacilli. Results: No significant differences were found in the DMFT, dmft scores or community periodontal index (CPI) scores between the cases and controls. However, there was a positive correlation between DMFT and dmft scores (r = 0.83, P < 0.0001) in both the cases and controls. In asthmatic patients who took their medication 3 times a day or more, the level of MS and lactobacilli was significantly higher (P = 0.014 and P = 0.008, respectively) compared with other asthmatic patients. Patients with severe asthma had significantly lower salivary flow rate levels than other asthmatic patients (P = 0.040), while patients taking a combination therapy of anti-asthmatic drugs with corticosteroids had higher levels of lactobacilli compared with patients using other medications (P = 0.02). Conclusions: The frequency of taking asthma medication, the severity of asthma and the use of combination therapy can significantly alter the salivary characteristics in asthmatic children. Key words: asthma, caries, children, saliva Oral Health Prev Dent 2013;11:113-120 doi: 10.3290/j.ohpd.a29366
A
sthma is a chronic airway disease characterised by inflammation and bronchoconstriction (Mannino et al, 1998; Steinbacher and Glick, 2001). It is a
Assistant Professor and Consultant Pediatric Dentist, Preventive Dental Sciences Department, Faculty of Dentistry, King Abdulaziz University, Jeddah, Saudi Arabia.
b
Assistant Professor, Preventive Dental Sciences Department, Pediatric Dentistry Division, Faculty of Dentistry, King Abdulaziz University, Jeddah, Saudi Arabia; Pedodontic Department, Faculty of Dental Medicine for Girls, El Azhar University, Cairo, Egypt.
c
Associate Professor and Consultant Pediatric Dentist, Faculty of Dentistry, Alexandria University, Alexandria, Egypt.
d
Demonstrator, Preventive Dental Sciences Department, Faculty of Dentistry, King Abdulaziz University, Jeddah, Saudi Arabia.
e
Demonstrator, Preventive Dental Sciences Department, Faculty of Dentistry, King Abdulaziz University, Jeddah, Saudi Arabia.
Correspondence: Sumer Madani Alaki, Preventive Dental Sciences Department, Faculty of Dentistry, King Abdulaziz University, Jeddah, Saudi Arabia. Tel: +9662-640-1000, Fax: +9662-695-2847. Email:
[email protected] [email protected]
Vol 11, No 2, 2013
Submitted for publication: 08.03.11; accepted for publication: 17.05.12
a serious global health problem affecting more than 100 million people worldwide; moreover, the prevalence of asthma has increased in the past two decades (Mehta et al, 2009). In reports from The Swedish Council on Technology Assessment in Health Care (SBU), about 20% of children under two years of age and about 10% of schoolchildren are affected by asthma (Steinbacher and Glick, 2001). In Western countries, the prevalence of allergic disorders including asthma in children has increased to 41% (Kjellman, 1977; Hattevig et al, 1987; Varjonen et al, 1992). Multiple causative factors including familial, infectious, allergenic, socioeconomic, psychosocial and environmental have been reported. The inflammatory response in the lungs can be triggered by various environmental factors, including viral infection, exercise, tobacco smoke, pets, dust, moulds
113
Alaki et al
and pollen. In susceptible children, these triggers cause swelling and narrowing of the airways characterised by airway hyper-responsiveness, airflow limitation and respiratory symptoms, which are most commonly manifested as coughing or wheezing and chest tightness (Harik et al, 2004). In Saudi Arabia, several studies have shown that the prevalence of bronchial asthma is continuously rising (Al Faryh et al, 2001; El-Sharif et al, 2003; Al-Rubaish, 2011). The studies have revealed an increased exposure to environmental factors such as tobacco smoke and indoor animals in Saudi homes. It seems that the continuing changes in contemporary life may well have contributed to the increased prevalence of asthma in this country. Recently, asthma treatment guidelines have stressed assessing levels of ‘asthma control’. Thus, treatment is directed primarily at achieving optimal asthma control by reducing impairment and eliminating risk. The goal of asthma medication is to provide symptomatic control with normalisation of lifestyle and to return as much pulmonary function as possible (Reed, 2006). Asthma medication can be delivered orally, parentrally, via inhalation or through a combination mode. Inhaled administration of an aerosolized drug is frequently preferred to other routes because of its ability to be administered directly to the airway. Another advantage is that a lower dosage than other systemic medication is required, especially for children (NIH, 2006). As the prevalence of asthma rises in the paediatric population, it is necessary to examine how this disease affects other areas of health care, most notably oral health. Studies in the literature investigating the effect of asthma on dental caries and periodontal status have shown inconsistent results. Some authors have reported a correlation between childhood asthma and dental caries in preschool children, whereas others have found no such connection. Eloot et al (2004) found that neither the length of the disease period, the medication nor the severity of the asthma disease had a significant effect on the risk of developing caries or gingivitis. Other studies by Reddy et al (2003), Ersin et al (2006) and Mehta et al (2009), however, concluded that asthma – through its disease status and its pharmacotherapy – carries some risk factors for caries development, including decreased salivary flow rate and pH. Furthermore, it has been demonstrated that the duration of illness and medication had significant influences on the risk of caries in asthmatics. In view of the considerations presented, it would be of great interest and value to study the severity
114
of dental caries and periodontal problems in children with bronchial asthma and to examine the correlation with the severity of asthma and the form of medication being taken. It would also be advisable to encourage the habit of more precautionary oral hygiene practices and regular monitoring of caries activity and periodontal health. Thus, the aims of this study were to assess and compare caries experience and salivary characteristics between asthmatic and healthy children and to investigate the effects of medication type, duration of use, mode of administration, times of use, frequency of use and severity of the disease on both caries experience and salivary characteristics in asthmatic children.
MATERIALS AND METHODS Study sample Ethical approval from the Deanship of Scientific Research (DSR), King Abdulaziz University, Jeddah, was given before selecting the sample. A total of 60 children between the ages of 5 and 13 years living in Jeddah, Saudi Arabia, were involved in the study. Thirty were asthmatic patients and 30 were medically fit children. The asthmatic children were randomly selected using an electronic filing system (R4) at King Abdul-Aziz University Hospital (KAAUH). This was done by reviewing all the dental files that were opened during the period from February 2010 to February 2011. The files in the R4 system comprise the general pool of patients including patients referred for orthodontic treatment. A list of all medically compromised patients was prepared by the administrative filing department at the university hospital. Then all the patients on the list were manually reviewed by a single reviewer in order to select only the patients diagnosed with asthma alone without any other medical disease, while other children whoe were diagnosed with asthma and other medical conditions were excluded. Finally, 30 asthmatic children were randomly selected. Another 30 healthy children were randomly selected from the system in the same manner described above. The selected children were given appointments at specialty clinics of the Paediatric Dentistry department at King Abdulaziz University Hospital. At each appointment, a consent form was given to one of the parents before dental examination and saliva sample collection.
Oral Health & Preventive Dentistry
Alaki et al
In the consent form, the parents were informed about the aim of the study, the dental examination and saliva sample for microbiological assessment. Additional data were gathered using a questionnaire, clinical examination and microbiological assessment. For the purposes of this study, asthmatic patients were patients who reported a physician’s diagnosis of asthma. To classify asthma, we used the classification of Shulman et al (2001) to classify the severity of asthma. Additionally, classification of asthma was based on parents’ information about the hospitalisation related to asthma in the last year. If the child was hospitalised twice or suffered 4 acute asthmatic attacks, this was considered severe asthma. If the child was hospitalised once or had 2 acute attacks or 3 wheezing episodes, the diagnosis was moderate asthma. Finally, the patient was diagnosed as mildly asthmatic if no history of hospitalisation existed and there had been one acute attack or 2 wheezing episodes.
Questionnaire One parent of each child was interviewed by a single examiner. The questionnaire included the following data: r Contact information (telephone number, file number) r Sociodemographic variables r Level of parents’ education r Dietary habits (frequency of sweets intake) r Oral hygiene habits (frequency of toothbrushing and parents’ role during brushing) r Medication types r Duration of taking the medication r Frequency of medication r Mode of administration r Onset of action r The times of taking medication r Severity of the disease
Dental examination The dental examination procedure was done by one of two examiners following the World Health Organization Criteria (WHO) (2003) by using a mouth mirror and a dental explorer under the incandescent light in the dental clinic. A tooth was considered ‘decayed’ if there was frank cavitation on the surface, ‘missing’ if the extraction was due to caries
Vol 11, No 2, 2013
and ‘filled’ if it had a restored carious lesion. Exfoliated, un-erupted teeth and those extracted for other reasons apart from caries were not included in the indices. Periodontal status was also assessed using the community periodontal index (CPI) (18). However, scores were restricted to 0 = healthy, 1 = bleeding and 2 = bleeding and calculus. No dental radiographs were taken. Intra-oral and extra-oral examinations for any abnormalities were done and reported. If a patient was found to need any urgent dental treatment, this was performed during the same appointment after complete data and saliva sample collection. Dental appointments with one of the two examiners were given whenever a child needed any further dental treatment. The two examiners were trained and calibrated and the reliability of each single examiner was assessed by re-examination of 6 children on a different day. There were 2 examiners in this study, and around 10% of patients in this study was examined twice by each examiner to determine intra-examiner reproducibility. For the first examiner, the intra-examiner reproducibility had a Kappa value of 98%. For the second examiner, the intra-examiner reproducibility had a Kappa value 96%.The inter-examiner reproducibility had a Kappa value of 92.6%.
Saliva collection All the patients were instructed not to eat or drink for at least 1 h before the appointment. They were also asked to refrain from toothbrushing on the morning of sampling. The sample collection was done by one of the two trained examiners. First, the patients were seated in an upright position; paraffin-stimulated whole saliva was collected for 3 min in a calibrated sterile tube. Then the salivary secretion rate was expressed as ml/min. Saliva samples were treated using a standardised CRT Ivoclar Vivadent kit, composed of CRT buffer and CRT bacteria tests (Ivoclar Vivadent; Schaan, Liechtenstein). The CRT Buffer Test was used to determine the buffering capacity of saliva using a colourimetric test strip. In order to measure the buffering capacity, the CRT Buffer Test was stripped from the package without touching the yellow test field. The entire yellow test field was moistened with saliva using a pipette. To determine the buffering capacity of saliva, the colour of the test field was compared with the colour samples after exactly 5 min of reaction time. High, medium and low salivary buffering capacities are indicated by blue, green and yellow
115
Alaki et al
test fields, respectively. The saliva collected for the CRT Buffer Test was also used for the CRT Bacteria Test. The agar carrier was removed from the test vial and a NaHCO3- tablet was placed at the bottom of the vial. Using a pipette, both agar surfaces were moistened with saliva. The agar carrier was placed back into the vial and closed tightly. After incubation at 37°C for 48 h, the density of Mutans streptococci and Lactobacillus colonies was assessed by both investigators using the corresponding evaluation pictures provided with the kit. The presence of bacterial colonies over 105 cfu (colony forming units) indicates a high risk for dental caries.
Table 1 The DMFT (permanent teeth) and dmft (deciduous teeth) scores for cases and controls Group
N
Mean
Case
30
2.1667
Control
30
1.9667
Case
30
8.9667
Control
30
8.0333
DMFT
0.76
dmft
0.59
Table 2 Salivary characteristics among cases and controls Salivary characteristics
Statistical analysis
Cases n (%)
Controls n (%)
Salivary flow rate (ml/min) 1.6
5 (16.7)
4 (13.3)
Buffering capacity High
19 (63.3)
21 (70)
Moderate
9 (30)
7 (23.3)
Low
2 (6.7)
2 (6.7)
Mutans streptococci
RESULTS The study sample consisted of 60 children, of which 30 (50%) were asthmatic. Among the asthmatic children, 17 (56.7%) were boys and 13 (43.3%) were girls. The control group consisted of 18 (60%) boys and 12 (40%) girls. The results show that 42.4% of fathers in the sample had achieved higher than highschool education, while 33.3% of mothers were found to have done so. 62.1% of all mothers were not employed outside the home. Sugar intake per day was relatively high, with a regular consumption of more than 3 times a day for 37.9% of the children and 2 to 3 times a day for 36.4%. In relation to brushing frequency, 40.9% brushed their teeth once a day, 33.3% twice a day, 12.1% more than twice a day and nearly 4.5% did not brush their teeth at all. The mean DMFT score was 2.16 for cases and 1.96 for controls, while the mean dmft score for asthmatic patients was 8.96 and 8.033 for healthy children (Table 1). No significant differences in the DMFT or dmft scores were found between cases and controls (P = 0.76 and P = 0.59, respectively). Most of the children in the sample had healthy gingival tissues. Intra-oral and extra-oral examina-
116
High
17 (56.7)
15 (50)
Low
13 (43.3)
15 (50)
High
21 (70)
10 (33.3)
Low
9 (30)
20 (66.7)
Lactobacilli
tions were normal except for one child who had trauma to the upper lip and three children who had intraoral abscesses. No significant differences in the CPI scores between cases and controls were found. The salivary characteristics of children in the sample including flow rates, buffering capacity, MS level and lactobacilli level are presented in Table 2. No significant differences were found in the salivary characteristics between cases and controls except for the lactobacilli level. Asthmatic patients had significantly higher lactobacilli levels compared with healthy children (P = 0.004).
Oral Health & Preventive Dentistry
Alaki et al
Table 3 Relationship between salivary characteristics and severity of asthma Classification of asthma Severe Moderate Mild
Salivary flow rate (ml/min)
Mutans streptococci (CFU)
Buffer
Lactobacilli (CFU)
>1
1-1.5
1
1-1.5
