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Table of Contents   
ORIGINAL RESEARCH  
Year : 2019  |  Volume : 30  |  Issue : 5  |  Page : 670-677
Evaluation of oral health of 6 to 10-year-old asthmatic children receiving bronchodilator through inhaler


1 Department of Pedodontics and Preventive Dentistry, University College of Medical Sciences and GTB Hospital, New Delhi, India
2 Department of Pediatrics, University College of Medical Sciences and GTB Hospital, New Delhi, India

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Date of Submission16-Sep-2014
Date of Decision13-Jun-2015
Date of Acceptance27-Sep-2017
Date of Web Publication18-Dec-2019
 

   Abstract 


Aim: The aim of this study was to evaluate the oral health status in 6 to 10-year-old asthmatic children receiving bronchodilator (salbutamol, salmeterol, etc.) through inhaler and compare them with nonasthmatic healthy children. Settings and Design: The present study was carried out at pediatric and pedodontic department and neighboring government school. It was an observational and case–control study. Statistical Analysis: All data were analyzed using SPSS 20.0 software program and presented as mean ± standard error of mean. Chi-square test was used for the categorical data between groups. Numerical data were analyzed by Mann–Whitney U-test and t-test. Kruskal–Wallis test was performed for comparisons of median value of decayed, missing, filled surface and Decayed, Missing, Filled Surface (dmfs and DMFS) for different variables within asthmatic group. Mann–Whitney U-test for multiple comparisons and P value was adjusted according to Bonferroni correction. Negative binomial analysis was used to calculate adjusted dmfs and DMFS, and univariate analysis of variance was used for adjusted mean plaque and gingival index. Materials and Methods: The study group composed of 70 asthmatic and 70 nonasthmatic children with the same age and social background aged between 6 and 10 years old. Oral health status was assessed using caries, plaque, and gingival index. Dental caries examination was done using the WHO criteria (1997), plaque index by Silness and Loe in 1964 and gingival health by Loe and Silness in 1963. Results: The children in the asthmatic group had significantly higher caries prevalence, severity of dental plaque, and gingivitis compared with the nonasthmatic group. Plaque accumulation and gingivitis increased significantly as severity and duration of asthma increased. Conclusions: Bronchial asthma had an overall deleterious effect on caries prevalence and severity, plaque, and gingivitis on primary and permanent teeth.

Keywords: Asthma, bronchodilator, inhaler

How to cite this article:
Kumar S, Kalra N, Tyagi R, Faridi M M, Khatri A, Satish V N. Evaluation of oral health of 6 to 10-year-old asthmatic children receiving bronchodilator through inhaler. Indian J Dent Res 2019;30:670-7

How to cite this URL:
Kumar S, Kalra N, Tyagi R, Faridi M M, Khatri A, Satish V N. Evaluation of oral health of 6 to 10-year-old asthmatic children receiving bronchodilator through inhaler. Indian J Dent Res [serial online] 2019 [cited 2020 Aug 5];30:670-7. Available from: http://www.ijdr.in/text.asp?2019/30/5/670/273431



   Introduction Top


Asthma is a chronic airway disease characterized by inflammation and bronchoconstriction.[1],[2] It is one of the most common chronic diseases and a serious global health problem affecting more than 300 million people worldwide and most of the countries reported that the prevalence has increased during the past two decades.[3] In India, the prevalence of asthma is 15–20 million.[4] Although it affects people of all age groups, peak prevalence exists between ages of 6 and 11 years.[5] In childhood asthma, there is a male-to-female ratio of 2:1 although the disease in adults does not have the same wide disparity in prevalence between the two gender groups.[6]

Studies investigating the association of asthma and dental caries are conflicting. While similar caries prevalence with healthy individuals is reported in some studies.[7],[8] Most of the others have suggested that asthmatic children are at higher risk for oral disease than nonasthmatic children due to either their disease or their pharmacotherapy.[9],[10],[11]

It is suggested that increase in caries prevalence in asthmatic children was associated with prolonged use of β2-agonist which leads to decrease in salivary flow and salivary pH. This salivary flow reduction is associated with concomitant increase in Lactobacillus and Streptococcus mutans, the pathogenic microorganism of dental caries.[12]

Asthmatic participants also showed a decrease in output per minute of total protein, amylase, hexosamine, salivary peroxidase, lysozyme, and secretory IgA in stimulated parotid saliva. These components of saliva are protective in nature for oral health.[10]

Asthmatic patients also experience gingivitis that could be attributed to an altered immune response and dehydration of oral mucosa due to mouth breathing.[13] It is found that in asthmatic children, a large proportion of inhaled drug is retained in the oropharynx, ranging from 80% with metered dose of inhaler and 60% with dry-powder inhaler with extension tube. In addition, some dry-powder inhaler and pressurized metered-dose inhaler contain sugar so that the patient can tolerate the taste of the drug when it is delivered. Frequent oral inhalation of sugar combined with a decrease in salivary flow rate and a decrease in pH of saliva may contribute to increase in caries.[14]

The aim of the study is to investigate the caries status, oral hygiene status, and gingivitis in asthmatic children and relation with the severity of disease, duration, and type of medication used.


   Materials and Methods Top


The study consisted of two groups: asthmatic group and nonasthmatic group. Seventy asthmatic children aged 6–10 years old from both genders who were using inhaler for more than 1 year were included in the study from outpatient settings and emergency of the department of pediatrics. Children with any systemic illness along with asthma were excluded from the study. Nonasthmatic healthy children, aged 6–10 years, comparable in age, gender, and socioeconomic status with asthmatic children were recruited from neighboring government school located within 2 km range of hospital. First, a list of children was made from all the sections of class first to third within the age group of 6–10 years for a total of 372 children. Of these 372 children, 16 were dropped due to some systemic illness. A simple random sampling was done for remaining 356 children to get the sample size of 70 children.

Ethical clearance was taken from the Institutional Ethical Committee, and a written informed consent was obtained from parents or caretakers of asthmatic as well as nonasthmatic children.

A detailed medical history of asthmatic children was recorded which included history of asthma, i.e. duration of asthma, severity, type of medication (bronchodilator, corticosteroids, or combination both), duration of medication, mode of receiving drug (inhaler), and any other diseases. Asthmatic children were classified according to severity of asthma into mild intermittent, mild persistent, moderate persistent, and severe persistent with the help of senior pediatrician using standard classification.[15],[16] Children's weight and height were recorded with electronic weighing machine and height-weight chart, respectively, to exclude the malnourished children using height and weight criteria.[17] Personal data about dental status included: tooth brushing frequency, use of fluoride toothpaste or mouthwash, frequency of sugar intake in between meals, and mouth breathing habit.

Clinical examination

Intraoral clinical examination was done for caries status decayed, missing, filled surface/Decayed, Missing, Filled Surface (dmfs/DMFS), dental plaque accumulation, and gingivitis using the standard indices in both the groups. Calibration between both guides and investigator conducted before study, and kappa value of 0.95 for intra-examiner reproducibility and 0.87 for inter-examiner reproducibility was found.

  • Caries status: This was measured by dmfs index for deciduous teeth and DMFS index for permanent teeth given by the WHO, Oral Health Survey, Geneva in 1997.[18] No radiographs were taken and decay was recorded at the level of cavitation
  • Plaque status: This was measured using dental plaque index given by “Silness and Loe” (1964)[19]
  • Gingival status: This was measured using gingival index given by “Loe and Silness” (1963).[20]


All children were examined for mouth breathing habit using mirror test to find the association of mouth breathing with oral health in asthmatic children.

After oral examination, dental health information and brushing demonstration were given to all children. All asthmatic children were taught about the deleterious effect of inhalers, how to use them and what precautions should be taken. All teeth those requiring treatment were taken up for the treatment as suitable.

Statistical analysis

All data were analyzed using SPSS 20.0 software (IBM Corp, US) program and presented as mean ± standard deviation. Chi- squaretest was used for the categorical data (gender, socioeconomic status, etc.) between groups. Numerical data such as median dmfs, median DMFS, mean plaque, and mean gingival index were analyzed by Mann–Whitney U-test and t-test in asthmatic and nonasthmatic groups. Kruskal–Wallis test was performed for comparisons of median value of dmfs and DMFS for different variables within asthmatic group, for example, severity, medication, duration of medication used, etc., and Mann–Whitney U-test for multiple comparisons, and P value was adjusted according to Bonferroni correction. Analysis of variance test was performed for comparisons of mean values of plaque and gingival index for different variables within asthmatic group, for example, severity, medication, duration of medication used, etc., and Tukey's test for multiple comparisons.

Mann–Whitney U-test and unpaired t-test were performed to observe if, any association was found between various confounding factors affecting oral health status and asthma. The critical level for statistical significance was set as P < 0.05. Negative binomial analysis was used to calculate adjusted dmfs and DMFS, and univariate analysis of variance was used for adjusted mean plaque and gingival index.


   Results Top


A total of 140 children, 70 asthmatics and 70 nonasthmatics, were recruited in the study. The mean age and gender distribution of asthmatic and healthy children were similar between groups (χ2, t-test). The mean ages for asthmatic and nonasthmatic children were 8.07 ± 1.49 and 7.26 ± 0.85, respectively. There were 36 males in asthmatic group and 28 males in nonasthmatic group.

The children in the asthmatic group had significantly higher caries prevalence 98.6% in as compared to nonasthmatic children 62% (χ2-test, P < 0.001). The mean dmfs and DMFS were significantly higher in asthmatic children as compared to nonasthmatic children (P < 0.001). Plaque and gingival scores were significantly higher in asthmatic group when compared with nonasthmatic group (P < 0.001) [Table 1].
Table 1: Comparison of mean decayed, missing, filled surface, mean Decayed, Missing, Filled Surface, plaque index, and gingival index in asthmatic and nonasthmatic children

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During the study period, only one case of mild intermittent asthma was observed, so it was eliminated due to statistical reasons, and analysis was done on 69 asthmatic participants. The significance level was set to P < 0.02 due to Bonferroni correction. Results showed that mean dmfs scores were significantly increased (P = 0.006) as severity of asthma increased. The mean DMFS increased as severity increased from mild to moderate persistent asthma but further declined in children with severe persistent asthma, and results were insignificant. When comparing mild versus moderate asthma, mean DMFS score was significantly increased, whereas in mild versus severe and moderate versus severe asthma, mean dmfs scores were increased significantly with P = 0.000 and 0.011, respectively [Table 2].
Table 2: Comparison of mean decayed, missing, filled surface and mean Decayed, Missing, Filled Surface index according to severity of asthma

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ANOVA test was used for statistical analysis and Tukey's test was used for multiple comparisons for plaque and gingival scores according to severity pattern of asthma. Plaque and gingival scores increased as severity of asthma increased. When comparing mild versus moderate asthma, plaque and gingival scores increased significantly, i.e., P = 0.013 and 0.02, respectively. In comparison of mild versus severe asthma, only plaque score was significantly increased (P = 0.013). When comparing moderate versus severe asthma, plaque score increased and gingival scores decreased, but results did not achieve statistically significant with P = 0.719 and 0.720, respectively [Graph 1].



Mann–Whitney test was used for comparing group taking bronchodilator alone with those taking combination of bronchodilator and corticosteroids. Results showed that mean dmfs and mean DMFS values were higher in asthmatic children when they took combination of bronchodilator and corticosteroids. However, these results did not reach the significance level as P > 0.05 [Graph 2].



Mean plaque and gingival scores increased when asthmatic children took combination of bronchodilator and corticosteroids as compared to asthmatic children who took only bronchodilator, but results were highly significant in plaque score (P < 0.001) and significant in gingival scores (P < 0.05) [Graph 3].



Mean dmfs and mean DMFS scores increased significantly (P < 0.05) as duration of inhaler used was increased. When comparing duration of inhaler used of ≤2 years with more than 2 years and ≤4 years, no significant increase in dmfs and DMFS was observed. It is an intergroup comparison between inhaler used for > 4 year with other two i.e group using inhaler < 2 year and > 2 to < 4 year [Table 3].
Table 3: Comparison of mean decayed, missing, filled surface and Decayed, Missing, Filled Surface according to duration of inhaler used in asthmatic children

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Mean plaque and gingival scores increased as duration of inhaler used increased from 1 to 4 years but further decreased as duration increased more than 4 years. Results were statistically nonsignificant (P > 0.05). Furthermore, when intergroup comparison among first two groups was done, no significant results were observed in plaque and gingival scores (P > 0.05) [Graph 4].



As dental caries is multifactorial disease, influence of asthma on dental caries after adjusting confounding variables such as age, gender, tooth brushing frequency, frequency of snacking, socioeconomic class, and mouth breathing habit was assessed using negative binomial model with log link. [Table 4] and [Table 5] show adjusted mean dmfs and DMFS based on negative binomial regression analysis after adjusting confounding variables.
Table 4: Adjusted mean decayed, missing, filled surface based on negative binomial regression analysis after adjusting confounding variables

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Table 5: Adjusted mean Decayed, Missing, Filled Surface based on negative binomial regression analysis after adjusting confounding variables

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Both dmfs and DMFS scores were statistically highly significant (P < 0.001) in asthmatic children as compared to nonasthmatic children after adjusting confounding variables. The relative risk ratio of dmfs and DMFS in asthmatic group was 186% and 442% higher, respectively, than nonasthmatic group after adjusting confounding variables.


   Discussion Top


The present study was a case–control study conducted on asthmatic patients to assess the possible association of asthma and its management with oral health. The prevalence of dental caries was 98.6% in asthmatic children that was significantly high as compared to nonasthmatic children with caries prevalence of 62% in similar age group. The mean dmfs and DMFS scores were found statistically significant (P < 0.001) in asthmatic group when compared with nonasthmatic group [Table 1]. The mean dmfs and DMFS scores analyzed after adjusting the confounding variables were also found statistically significant (P < 0.001) [Table 4] and [Table 5]. These results were in agreement with Ersin et al.,[11] but the level of significance was more in our study with P < 0.001 as compared to their study with P < 0.05. Reddy et al.[21] showed 78.31% of caries prevalence in mixed dentition in asthmatic children which was less as compared to our results, i.e., 98.6%. These results showed that asthmatic children are at higher risk for caries development than nonasthmatic healthy children, as proven by some other studies like Khalilzadeh et al.[22] and Mazzoleni et al.[23]. However, Meldrum et al.[7] and Shulman et al.[8] reported that asthmatic children did not have a higher caries experience than controls. Meldrum et al.[7] had shown that there was no significant difference in 3-year net caries increment between asthmatic and control group. The possible cause of an increase in caries prevalence has been related to the use of β2-agonist in the treatment of asthma which leads to reduction in the salivary flow. Ryberg et al.[10] reported a decrease in the secretion rate of stimulated whole saliva and parotid saliva in asthmatic patients as well as lower output of salivary components such as salivary IgA, lysozyme, amylase, and peroxidase activity compared to nonasthmatics. All these factors play an important role in the antibacterial action of saliva and are protective. As these protective factors decrease, caries production is likely to rise as reported their study. Laurikainen et al.[24] observed a statistically significant difference in the mean stimulated salivary flow rate between asthmatic and control group. A reduced salivary flow is accompanied by concomitant increase in Lactobacilli and Streptococcus mutans level in oral cavity and can increase caries risk in an individual.[12] On the contrary, Hyyppä[25] demonstrated no difference in salivary flow between asthmatic and healthy controls.

Another potential factor attributing to caries development in asthmatic patients could be a decrease in plaque and salivary pH caused by inhalers. Kargul et al.[14] found a reduced pH among asthmatic adolescents who were using asthma inhalers. Tootla et al.[26] found that most dry-powder inhaler produced pH value below 5.5 which is near critical pH, indicative of their potential to dissolve enamel hydroxyapatite. These findings were in agreement with those of O'Sullivan et al.[27] On the other hand, anin vitro study by Tootla et al.[28] could not demonstrate the cariogenic/acidogenic potential of inhaler.

In the present study, the prevalence of dental plaque was 100% in both the groups. The mean plaque score was significantly high (P < 0.001) in asthmatic group as compared with nonasthmatic group [Table 1]. This was similar to the finding of Mehta et al.[29] and Hyyppä[30] where higher plaque score was recorded in asthmatics. Ersin et al.[11] reported increased plaque scores in asthmatic as well as control group, but they did not differ statistically. Stensson et al.[31] could not find difference in plaque formation rate between asthmatic and control group, and they explained it on the basis of good oral hygiene in both the groups.

Magnusson et al.[32] and Kousvelari et al.[33] reported that the availability of biological component is a decisive factor in salivary reduction in asthmatic patients. This decreased salivary flow output causes lowering of antibacterial component in saliva that favors bacterial colonization and plaque formation. This altered activity of biological components explains the higher plaque formation in asthmatic children.

The mean gingival index scores were significantly high (P < 0.001) in asthmatic group as compared with nonasthmatic group [Table 1]. This is in agreement with the Mehta et al.[29] and Stensson[31] who reported higher gingival scores in asthmatics when compared with healthy controls. Hyyppä et al.[13] observed that asthmatic children had more severe gingivitis than their healthy controls. They explained that asthmatic patients had habit of frequent mouth breathing, and during asthma attack, they generally tend to breathe through their mouth causing gingivitis. Hyyppä et al.[13] also suggested that corticosteroids used for the treatment of asthma alter the immune response of oral cavity causing increase in arginine aminopeptidase activity, an enzyme involved in inflammatory reaction that could be the reason of gingivitis in asthmatic children.

It also has been suggested that asthmatic children exhibit more calculus than do healthy children.[34] This possibly is caused by increased levels of calcium and phosphorus found in submaxillary and parotid saliva in children with asthma.[35],[36]

In our study, gingivitis could be possibly due to combination of all three factors involved in gingival inflammation, i.e., high plaque accumulation, presence of mouth breathing, and use of corticosteroids for the treatment of asthma.

The mean dmfs increased significantly (P = 0.006) as severity of asthma increased, whereas mean DMFS increased significantly from mild to moderate asthma, but this trend was reversed in children with severe asthma. The reverse trend in mean DMFS in severe asthmatic children could be explained as that very few patients comprised the severe asthmatic group that could not be considered as a true representation of sample group [Table 2].

Our results were in accordance with Shulman et al.[8] and Reddy et al.[21] who found that asthmatic children had higher caries prevalence and it increased with the severity of disease due to increase in dosage and frequency of medication. Whereas, Eloot et al.[37] and Ersin et al.[11] found that severity of asthma had no significant influence on the risk of caries in asthmatic children.

In the present study, dental plaque accumulation and gingivitis increase significantly as severity of asthma increased (P < 0.05). This could be explained that as the severity of asthma increases, dosage and frequency of anti-asthmatic medications increase, which leads to greater reduction in salivary flow that diminishes the cleansing and flushing action of saliva consequently resulting in more plaque accumulation. Similarly, according to severity of asthma, intensity of mouth breathing increased that leads to severe gingivitis.

The present study showed that mean dmfs value increased as duration of inhaler use increased from <2 years to ≤4 years, but the same increasing trend was not preserved as duration of inhaler used further increased to more than 4 years in primary teeth.

Milano et al.[38] showed that caries prevalence decreased in asthmatic children who were using inhalers for more than two years and they explained it as better disease management over time. The same may be true for the present study in primary dentition where a decline in caries was observed on the use of inhaler for more than four years.

In permanent teeth, caries prevalence, i.e., mean DMFS increased significantly (P < 0.002) as duration of inhaler use increased. This may be explained in terms of fewer children using inhaler for longer duration.

Our results showed that dental plaque accumulation and severity of gingivitis increased according to duration of inhaler use from one to four years, i.e., an increasing trend was seen, but this trend was declined as duration of inhaler increased more than four years. The point of turning was four years. Reason for such decline could be explained either by fewer number of sample size in group of children used inhalers for more than four years or by better management of disease over time in the same manner as prevalence of dental caries.[38]

The mean dmfs and DMFS were high in children using combination of bronchodilator and corticosteroids, but difference between them was insignificant (P > 0.05). Similarly, dental plaque accumulation and severity of gingivitis were increased in asthmatic children using combination of bronchodilator and corticosteroids as antiasthmatic medications, but their results were highly significant (P < 0.001). The reason for such results could be explained by the fact that corticosteroid itself has deleterious effect on oral health, for example, altered immune response and oral mucosal changes. Kargul et al.[14] showed that along with deleterious effect of medication, other constituents of inhaler such as lactose affect oral health. In contrast, Ersin et al.[11] and Mehta et al.[29] found no significant correlation between different types of antiasthmatic medication and oral health status.


   Conclusions Top


From the present study, the following conclusions were drawn:

  • The prevalence of dental caries, dental plaque, and gingivitis was higher in asthmatic children as compared to nonasthmatic children
  • The prevalence and severity of dental caries was significantly higher in asthmatic children as compared to nonasthmatic children
  • The prevalence of dental plaque was higher in asthmatic as well as nonasthmatic children. Severity of dental plaque was significantly higher in asthmatic children as compared to nonasthmatic children
  • The prevalence of gingivitis was higher in asthmatic children, but results were statistically nonsignificant. The severity of gingivitis was significantly higher in asthmatic children as compared to nonasthmatic children.


Recommendation

Asthmatic children need to be put on preventive schedule to counter the ill effect of asthma and its medication. Constant monitoring by pediatric dentist and general pediatrician may help in declining the effect of disease. The asthmatic children should receive oral health education and proper technique of using inhaler.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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Correspondence Address:
Dr. Rishi Tyagi
Department of Pedodontics and Preventive Dentistry, University College of Medical Sciences and GTB Hospital, Dilshad Garden, New Delhi - 110 095
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijdr.IJDR_593_14

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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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