Association between Asthma and Dental Caries amongst 12-15 Years Old Children : A School-Based Cross-Sectional Study in Karachi , Pakistan

Objective: The study aimed to determine an association between dental caries and asthma among 12 to 15 years old children. Methods: This is a school-based cross-sectional study conducted from January to February 2016. A random sample of 544 children aged 12 15 years were enrolled from five private schools of Karachi. Dental caries was assessed using DMFT Index (Decayed, Missing, Filled teeth). The main exposure variable was asthma and information on it was collected through the International Study of Asthma and Allergies in Childhood (ISAAC) questionnaire. Results: The data was analyzed using Cox Proportional Hazard algorithm. Crude and adjusted prevalence ratios with 95% CI were reported. Total 554 children, 306 (56.3%) boys and 43.7% girls participated in the study. Mean age of children was 13.2 ± 0.05 years. Total number of children with DMFT > 0 was 30.5%. The decayed component contributed largely (22.8%) to the DMFT score. Overall prevalence of asthma was 20%. Prevalence of caries in asthmatic children was 28.4% as compared to 31% among non-asthmatic children. Adjusted prevalence ratio of dental caries in asthmatic children was 0.8 (95% CI 0.6 1.3) after adjusting for carious food intake, age, oral hygiene index and dentist visit; the association between asthma and dental caries turned out to be in-significant. There was significant interaction between maternal education and consumption of cariogenic food and also between child’s age and oral hygiene (p-value < 0.1). Conclusions: There was no association observed between asthma and dental caries among the children examined in this study.


Introduction
Asthma is a common respiratory disease of childhood [1]. Approximately 300 million individuals globally suffer from asthma [2]. International Study of Asthma and Allergies in Children (ISAAC) surveyed 1.2 million children from 98 countries and reported that prevalence of asthma is 14.1% among 13 -14 years old children [3]. The overall prevalence of asthma in Pakistan among 3 -17 years old is around 10.2% [4]. According to a Pakistani study, the prevalence of physician diagnosed asthma in school-going children aged 3 to 16 years is 15% [5]. Among pre-pubertal males, asthma is twice as common compared to females but later during adolescence, it affects both genders almost equally [6].
Dental caries is one of the most prevalent chronic diseases among children. It affects children both physically and psychologically. It influences the child's dietary intake impairing the growth and development [7]. Moreover, it also affects the self-esteem and quality of life of children [8] [9]. Caries ranks as the fourth most expensive disease to treat in some developing countries. The treatment cost of caries alone is higher than the total health budget of these countries [8].
Findings from the earlier studies on the association of dental caries with asthma are inconsistent; few have found positive association [10] [11] whilst others have not [12] [13] [14]. It has been suggested that asthmatics are susceptible to developing dental caries because the anti-asthmatic medications, the drug chemistry, its low pH [15], sugar content [16] and its effect on the salivary flow [17] may increase the vulnerability of caries among asthmatics. Moreover, asthmatics may consume more erosive drinks [18] or their practice of mouth breathing may be the reason for higher caries experience [19]. The possible reasons for conflicting results might be varying clinical presentations, diagnostic challenges and complex etiologies of the two chronic conditions. Alternatively, the lack of association in different studies could be attributed to insufficient sample size, inconsistent age groups, differences in the severity of asthma, use of other medications and participants belonging to different ethnicities.
Hence, it's important to identify association between the two diseases so that prophylactic strategies can be formulated to advocate for adherence to precautionary measures by asthmatics to avert undesirable effects on oral tissues. Therefore, the aim of this study was to determine an association between dental caries and asthma among 12 to 15 years old children.

Material and Methods
Across-sectional study was conducted from January to May 2016, among children aged 12 to 15 years from five private schools of high socio-economic areas in Karachi, Pakistan.
Inclusion and Exclusion Criteria of the participants Only those students were included who gave assent and their parents provided written consent. We excluded children who were suffering from respiratory diseases other than asthma or any other serious medical illness (e.g. epilepsy) that Asthma is a chronic condition due to inflammation of the air passages in the lungs. In an attack, the lining of the passages swell causing the airways to narrow, reducing the airflow in the lungs [21].

Definition of Outcome variable
Dental caries is localized destruction of susceptible dental hard tissues by acidic by-products from bacterial fermentation of dietary carbohydrates" [22] defined as the sum of all decayed, missing and filled teeth in the oral cavity assessed by clinical dental examination.
Data Collection procedure/tool A pretested self-administered questionnaire was used to collect the information on the potential risk factors of caries. Data regarding asthma (main exposure variable) was collected through the International Study of Asthma and Allergies in Childhood (ISAAC) questionnaire [24]. It comprised of eight items and each item is assigned a score from 0 to 2 and an overall score from 6 to 14 classifies the child as an asthmatic. The ISAAC questionnaire assesses the history of wheeze ever, asthma and dry cough, the frequency of wheeze attacks in the past 12 months, disturbance of speech or sleep related to wheeze and wheezing followed by exercise [24]. Participants oral examination was conducted to assess dental caries (the study outcome) by the qualified dentists. It was done using disposable dental kits which included mouth mirror, probe, tweezers and cotton swabs along with rechargeable flashlights.

Questionnaire
The questionnaire addressed child's gender, age, parents education, physician diagnoses of asthma, duration of asthma, type of medication administered and its frequency, family history of asthma and allergies, dietary habits (amount and frequency of intake of each carious food item using Food Frequency Questionnaire (FFQ) and oral hygiene behavior (assessed by tooth brushing frequency, dental visits and the reason for last visit). Additionally the mother of the children were interviewed via telephone regarding physician diagnoses of asthma, duration of asthma, past and current medication and its frequency, family history of asthma and mouth-breathing. Comprehensibility and clarity of questions were assessed through pre-testing.

Ethical Consideration
The study was approved by the Ethical Review Committee of the Aga Khan University Hospital. Children who were identified as asthmatics using ISAAC questionnaire were later contacted at home to inform their parents so that they could seek advice from a pulmonologist.

Data editing and entry
The filled questionnaires were edited by principal investigator and the data collectors both in field and office and any missing data were clarified immediately. Data was double entered by two data entry operators in Epi Info V.6.04. [26].
Statistical analysis STATA version 11.0 was used for data analysis. For categorical variables, frequencies and percentages were reported whereas for quantitative variables means and standard deviations were computed.
Factor analysis was used to analyze FFQ. The food score was divided into 4 categories depending on the consumption of junk food, sugary items and milk related products. Those children who consumed highest amount of cariogenic food belonged to food score category 4.
Prevalence Ratio (PRs) and their 95% confidence intervals (CIs) was calculated using Cox Proportional hazard algorithm. We used Cox proportional hazard algorithm and reported Prevalence ratio instead of Odds ratio as it is overestimated in cross-sectional studies when the outcome is frequent as in our case the prevalence of caries is 55% [27]. When every participant is assigned a constant risk period in Cox algorithm, the hazard rate ratio is equivalent to prevalence ratio in cross-sectional studies.
All variables having p-value less than 0.25 were included in the model. All biological plausible interactions were checked at 0.05 level of significance. Significant interaction was found between age & oral hygiene and mothers education & carious food consumption and kept in the model.
The prevalence of physician's diagnosed asthma was 11.9%. Approximately 6.6% children were identified as asthmatics on ISAAC tool and 1.5% children were revealed as asthmatics at interview with the parents. Thus, the overall prevalence of asthma was 20%. Wheeze during or after exercise was the most commonly reported symptom. Approximately 38% children had family history of asthma. One fourth of the children were allergic. About 58% children reported dust allergy (followed by 16% food allergy and 7% fur allergy).

Discussion
This study was aimed to evaluate an association between asthma and dental caries among school children aged 12 to 15 years studying at five private schools in   Karachi, Pakistan. We did not find any association between asthma and caries.
Our findings are comparable with the studies conducted by Eloot et al. [28], Meldrum et al. [13] Shulman et al. [29] and Bjerkeborn et al. [30] who also failed to detect any significant dissimilarity in caries experience between asthmatic and non-asthmatic children. On the contrary, findings from other studies suggest a relationship between asthma and caries [31]. The probable reason for inconsistent results regarding the association might be that asthma is seasonal in nature and it's difficult to examine any relationship of asthma with other diseases. The disease itself, its severity and medications fluctuate over time. In addition, it's difficult to assess the initiation of the disease. Moreover, a universally accepted definition of asthma does not exist. Estimation through symptoms is what surveys of asthma rely on. In our study too, we relied upon the information given by the students and their parents regarding the asthma status.
Caries prevalence in the present study was 30.5%. This is comparable to the study by Charani et al. [32] who reported a prevalence of 29% among children enrolled in schools located in similar affluent settings. Naidu et al. [33] reported e prevalence of 29.1% among 3 -5 years old Indians residing in Caribbean area.
Kutesa et al. [34] reported caries prevalence of 32.5% among 11 to 13 years old school children. Our estimates are lower than Mohiuddin et al. [35] who reported an overall prevalence of 69.6% among 6 to 12 year-old. Similarly, Abbas et al. [36] who reported 64.6% prevalence of caries among 11 to 16 year old children of Karachi. A possible explanation for such low prevalence of caries among our study participants could be due to better awareness regarding oral hygienepractices and access to dental care as majority of our study participants belonged to high socio-economic status. They reported to have increased frequency of tooth brushing, availability of fluoridated toothpastes and above all educated parents, all of which add to the protection against dental caries [37]. In our study child's age, previous dental visits, oral hygiene index and cariogenic food consumption were significantly associated with the dental caries. Caries prevalence was higher in children who had visited a dentist than those who had not. This was due to the fact that children with carious teeth visited the dentist more often to get the required treatment [38].
Furthermore, variables such as oral hygiene, child's age, maternal education and cariogenic food consumption were effect modifiers in our study. The association of cariogenic food consumption and caries varies by the level of maternal education. The lower the educational status of the mother, the higher was the child's consumption of unhealthy cariogenic food. The mother's years of education had a direct relationship with the selection of healthy fruits and vegetables consumption among children [39].
Children aged 12 to 13 years old had very high debris scores in the oral cavity as compared to those aged 15 years. A probable reason for this improvement in oral cleanliness maybe due to the fact that young adults become more conscious about their appearance as they desired to be socially accepted. Open Journal of Epidemiology The duration of asthmatic medications had no effect on the caries experience.
These results were similar to the finding from Eloot et al. [28] who reported that length of the disease or medication of asthma has no significant effect on the caries development. Ersin et al. [17] demonstrated a positive correlation between duration of asthma and S. mutans count in saliva and a negative relationship between duration of medication and pH of saliva among individuals having caries.
Another finding of the present study is that the type of medication used (inhaler or syrup) or its dosage has no effect on dental caries. This finding is in agreement to Eloot et al. [28]. However, on the contrary, Reddy et al. [40] reported that caries prevalence was the highest among children taking medication in the form of syrup. Moreover, Tootla et al. [41] found that only lactose based dry powder inhalers lower the pH of saliva below 5.5, resulting in demineralization of enamel. Ryberg et al. [42] reported impaired salivary secretion in asthmatics up to 20% decrease in secretory rates of stimulated whole saliva. However, the results of these studies are not comparable to the present study as the children in our study were using oral anti asthmatic medications intermittently, most of them were on combination therapy and there were frequent alterations in the form and dosage of medication, so individual effect of drug could not be evaluated. In addition the most common form of medication was inhaler and very low proportion of children in our study were using syrups (only 3 regular users and 9 occasional users). In the present study, we did not find any association between caries prevalence and the severity of asthma.
The strengths of our study included data collectors who were blinded regarding the exposure status (asthma) of children at the time of caries examination. This prevented differential misclassification (information bias) on the exposure status. Moreover, we reported prevalence ratios (PR) along with 95% CI. Methodologically, in a cross sectional study, PR is the recommended alternative to Odds Ratio, provided the outcome of interest is frequent [27].
There were some limitations too in the present study. Firstly, asthma was assessed via questionnaire rather than an objective measure like Spirometer. Since, asthma information was collected via questionnaire, thus it was mainly dependent on the parent or child ability to recall, and this could have led to s recall bias resulting in under or over reporting. To overcome this, we assessed asthma via ISAAC, physician diagnosis and parent interviews. Secondly, assessment of dental caries was done using DMFT index. No dental radiographs were employed for the logistic reasons. Thus, we might have under-estimated the actual magnitude of dental caries. However, reported sensitivity and specificity of DMFT Index is 1.0 and 0.65 to 0.80, respectively [43]. Moreover, this study was conducted in schools located in the most affluent areas of Karachi due to law and order situation of the country public schools were reluctant to grant permission for data collection. Socioeconomic status (SES) disproportionately affects dental caries so by taking a homogenous population in terms of SES, aided in controlling for the confounding at the design stage.

Conclusion
No statistically significant association could be found between asthma and dental caries. Longitudinal studies are needed to explore the role of asthma in dental caries.

Acknowledgements
We acknowledge all selected schools, students and parents for their participation and are indebted to the dentists of JSMU and our data collection team for their contribution. Sincere gratitude to Mr Iqbal Azam, Dr Nida Zahid, Dr Ana Nayani, Dr Faraz Siddiqui and Dr Tahir Yousufzai for their support and guidance.

Author's Note
WZ was the principal investigator of the study and conducted this study as part of her MSc Epidemiology & Biostatistics thesis project. She carried out the study conception, design, data analysis, interpretation of data and drafted the manuscript. MMK, has contributed in conception and design, and reviewing manuscript critically. SR was responsible for design, sample size estimation, data analysis, interpretation of data and reviewing the manuscript. FRK contributed in the design of the study and manuscript review. NZ read and approved the final manuscript.

Conflicts of Interest
None declared.

Data Sharing Statement
No additional unpublished data is available from the study. The data of this study is with the first author of the manuscript.

Funding
Department of Community Health Sciences, Aga Khan University provided the funding for the study.