DOI: 10.1111/j.1365-263X.2012.01243.x

children in Slovenia

Influence of anti-asthmatic medications on dental caries in

TOMI SAMEC1, BENNETT TOCHUKWU AMAECHI2, TADEJ BATTELINO3, UROS KRIVEC4

& JANJA JAN1

1Department of Cariology and Endodontics, Faculty of Medicine, University of Ljubljana, Ljubljana, Slovenia, 2Department

of Comprehensive Dentistry, University of Texas Health Science Center at San Antonio, San Antonio, TX, USA, 3Division of

Paediatrics, Department of Endocrinology, Diabetes and Metabolic Diseases, University Medical Centre Ljubljana, Ljubljana,

Slovenia, and 4Unit of Pulmonary Diseases, Division of Paediatrics, University Medical Centre Ljubljana, Ljubljana, Slovenia

International Journal of Paediatric Dentistry 2012

Objective. The study investigated the influence of

exposure to anti-asthmatic medications and of

various factors on the caries prevalence in chil-

dren in Slovenia.

Methods. The study population consisted of chil-

dren aged 2- to 17 years (n = 220) under treat-

ment for asthma, who had used anti-asthmatic

medications for at least 1 year; 220 controls were

matched for age. Caries status was determined by

the number of decayed, missing, and filled sur-

faces through clinical examination by two cali-

brated dentists using the International Caries

Detection and Assessment System-II scoring crite-

ria. Questionnaires completed by parents and data

Correspondence to:

T. Samec, Department of Cariology and Endodontics,

Faculty of Medicine, University of Ljubljana, Hrvatski trg 6,

SI – 1000 Ljubljana, Slovenia.

E-mail: tomi.samec@mf.uni-lj.si

� 2012 John Wiley & Sons Ltd, BSPD and IAPD

from the patients’ medical records provided infor-

mation on various confounding factors.

Results. Asthmatic children had significantly higher

(P £ 0.01) prevalence of caries on primary and

permanent teeth in all age groups, and the pro-

portion of caries-free children was significantly

smaller (P £ 0.05). In multivariate regression anal-

ysis, asthma diagnosis, child’s age, daily use of

inhaled glucocorticoids, length and frequency of

medicine application, spacer use, mouth rinsing

with water after medicine application, parents’

education, frequent food and drink consumption,

and frequency of toothbrushing were associated

with caries experience of asthmatic children.

Conclusion. Children with asthma who had used

anti-asthmatic medications had higher caries

experience in primary and permanent teeth.

Introduction

Dental caries is one of the most prevalent

chronic diseases worldwide. Caries lesion

forms through a complex interaction over

time between acid-producing bacteria and fer-

mentable carbohydrates and is also affected

by many host factors including saliva and

the inherent nature of the teeth. Risk of

dental caries development includes physical,

biological, environmental, behavioural, and

lifestyle-related factors, such as presence of

dental plaque, high numbers of cariogenic

bacteria, inadequate salivary flow, insufficient

fluoride exposure, poor oral hygiene, inap-

propriate sugar consumption, and usage of

various medicines1. The caries process is a

continuum result from many cycles of demin-

eralization and remineralization, which is the

body’s natural attempt of repairing caries

lesions2.

Asthma, on the other hand, is a chronic

lung disease that demonstrates reversible air-

way obstruction, inflammation of the airway,

and increased responsiveness of the airways

to stimuli. Asthma is a major global health

problem, and the prevalence is increasing in

most countries, especially among children3. It

is a leading cause of childhood hospitaliza-

tions4. The treatment of asthma starts with

avoidance to stimuli, but controlling the

symptoms with anti-asthmatic medicines is

the main component of most asthma treat-

ments. Pharmacological management of

chronic childhood asthma involves two main

categories of drugs: bronchodilators and anti-

inflammatory agents. Children with mild

1

2 T. Samec et al.

asthma often are managed only with inhaled

b2-agonist bronchodilators. Inhaled glucocor-

ticoids are effective anti-inflammatory agents,

recommended for use in children with mod-

erate to severe asthma3.

A link between oral diseases and the com-

monly used anti-asthma inhalant medications

has biological credibility. Decreased salivary

flow rate in asthmatic children and also

changes in saliva composition and its pH are

linked to the use of anti-asthmatic medica-

tions. This association was observed for

inhaled b2-agonists5,6 and in combination

with glucocorticoids7–12. They can thus

reduce the effect of saliva in the aid of protec-

tion against caries. Adolescents and young

adults with asthma showed lower plaque ini-

tial pH values and plaque pH drop after a

sucrose rinse compared to the control

group10,11. Associations between increasing

prevalence of caries13 and lower salivary flow

rate12,14 with increasing severity of asthma

were observed, most likely due to the

increased dosage and frequency of medication

required to treat more severe asthma.

Increased salivary levels of Streptococcus mutans

were observed in asthmatic children, and

they were proved to be an important risk fac-

tor for increased caries experience15.

Risk factor for higher caries experience in

asthmatic children can also be more frequent

consumption of sweet drinks and sweets

between meals16. The reason proposed is

lower saliva secretion and dry mouth, which

are present in asthmatic patients5–9, especially

those on glucocorticoids17. The increased sus-

ceptibility to dental caries can also be due to

the frequent use of anti-asthmatic medica-

tions containing fermentable carbohydrates.

The most common is lactose monohydrate,

and although it is one of the least cariogenic

sugars, this still can lead to increased dental

caries risk18.

The mode of anti-asthmatic medicine appli-

cation may be an important factor for caries

risk. It has been shown that most of the med-

icine is retained in the mouth or throat: 80%

when using controlled-dose inhaled and in

dry powder inhaled form and 60% when

using spacer19. To remove the retained

medication from the oropharyngeal region,

patients are advised to rinse their mouths

with water after medication use.

Epidemiological studies investigating the

effect of asthma on dental caries are conflict-

ing. The majority of the studies conclude that

asthmatic children have a higher dental caries

prevalence6,10,13,16,20–23, whereas some oppose

such conclusions5,24–27. The discrepancies

between the different studies can be

explained by different study populations,

sample sizes, methodological differences, dif-

ferences in disease severity, and anti-asth-

matic medications used. In the study of

Ryberg et al.5, children currently using only

b2-agonists were included, whereas Stensson

et al.10 included adolescents with only severe

and very severe asthma with daily glucocorti-

coid treatment for a minimum of 4 years. In

the study of Shulman et al.26 no significant

associations between asthma and higher prev-

alence of dental caries were found. In this

study, <45% of the children with severe

asthma were prescribed anti-asthmatic medi-

cation, and there is a possibility that despite

their doctor’s prescription, they did not take

medicines. Only a few children from the

moderate and severe asthma group would use

glucocorticoids, and only for a short duration.

The number of studies that investigate the

association between asthma and oral health

has increased in the last decade, but more

studies are needed, as asthma affects more

than 300 million people worldwide4. There-

fore, our main aim was to investigate the

influence of exposure to anti-asthmatic medi-

cations on the caries prevalence in children

in Slovenia. In addition, we aimed to assess

the influence of various factors, for example

glucocorticoid dose, length and frequency of

medicines application, sugar presence in med-

icines, spacer use, rinsing the mouth after

medicine application, child age, sex, dietary

habits, oral hygiene habits, time since last

dental visit, and parents’ education on dental

caries susceptibility.

Materials and methods

The study population consisted of 2- to 17-

year-old children (n = 220) under treatment

for chronic bronchial asthma at the University

� 2012 John Wiley & Sons Ltd, BSPD and IAPD

Anti-asthmatic medications and dental caries 3

Children’s Hospital, Ljubljana, Slovenia. The

study was approved by ethics committee at

the Ministry of Health in Slovenia. All the

parents gave written informed consent. To

have a more homogenous group by disease

severity, the asthmatic children must have

used anti-asthmatic medications daily for at

least 1 year. To be included in the study, they

had to have physician-diagnosed asthma.

Children suffering from additional diseases

such as heart diseases, gastro-oesophageal

reflux, chromosomal abnormalities, infectious

diseases, eating disorders, and frequent vomit-

ing were excluded from the study. Controls

were healthy children matched for age

(±6 months) who went to the University

Dental Clinic in Ljubljana, Slovenia. They

were treated by undergraduate students and

had their dental charts available. Children

had equal preventive treatment and educa-

tion. A total of 440 children were examined

(mean age, 8.5 ± 3.0 years, range, 2–17 years).

Dental examinations were carried out in

2008 at the University Dental Clinic in a den-

tal chair under artificial light by two cali-

brated dentists using a standard dental mirror

and rounded dental probe. The dental exam-

iners were blinded to children with and with-

out asthma. We used a subtler, newly

developed International Caries Detection and

Assessment System-II (ICDAS II) scoring cri-

teria28, which measures the disease process at

its different stages. Caries status was deter-

mined by the number of decayed [non-cavi-

tated primary (d1) and permanent (D1), and

cavitated primary (d2) and permanent (D2)],

Table 1. International Caries Detection and Assessment System-II

Score Clinical criteria description

0 Sound tooth: no evidence ofwith developmental defects(attrition, abrasion and eros

1 First visual change in enameair-drying, which is not or h

2 Distinct visual change in enalesion must still be visible w

3 Localized enamel breakdown4 Underlying dark shadow from5 Distinct cavity with visible de6 Extensive distinct cavity with

possibly reaching the pulp.

� 2012 John Wiley & Sons Ltd, BSPD and IAPD

missing (M), and filled (f ⁄F) surfaces [primary

(dfs) and permanent (DMFS)] teeth. The basic

codes range from measurement of the first

visible carious change in enamel caused by

carious demineralization (code 1) to extensive

cavitation with visible dentin (code 6) as

shown in Table 1. Only permanent teeth

extracted as a consequence of dental caries

were marked as missing. Radiograph was not

included in the examination. Calibration

among the examiners was conducted prior to

the study by a cariologist, who is experienced

in caries diagnosis. Intra- and inter-examiner

reproducibility was tested on 10% of the chil-

dren.

Questionnaires completed by parents and

data from the patients’ medical records pro-

vided information on demographics, medical

history, medication usage, dietary history,

oral hygiene habits, fluoride exposure, and

for asthmatic children also on type, dose, fre-

quency, length and mode of medicine appli-

cation. For the glucocorticoid dose, we used

the dose the children had been using for the

previous 6 months.

For the purpose of the study, the popula-

tion was divided into three age groups. The

first age group was composed of 2- to 6-year-

old children (n = 120), the second age group

of 7- to 12-year-old children (n = 282), and

the third age group of 13- to 17-year-old chil-

dren (n = 38). Dental caries experience on

primary teeth was recorded in the first and

second age groups only, and on primary and

permanent teeth in the second and third age

groups.

(ICDAS II) scoring criteria.

caries after prolonged air-drying (5 s), surfaces(enamel hypoplasia, fluorosis), tooth wear

ion), and extrinsic or intrinsic stains will be recorded as sound.l: opacity or discoloration is visible after prolongedardly seen on a wet surface.mel: opacity or discoloration distinctly visible when wet,hen dry.owing to caries with no visible dentin or underlying shadow.dentin with or without localized enamel breakdown.

ntin: visual evidence of demineralization and dentin exposed.visible dentin with more than half of the tooth surface involved or

4 T. Samec et al.

Data on caries experience were presented

in primary teeth as d1fs (non-cavitated

decayed and filled surfaces), d2fs (cavitated

decayed and filled surfaces), d12fs (non-cavi-

tated, cavitated, and filled surfaces), and in

permanent teeth as D1MFS (non-cavitated

decayed, missing, and filled surfaces), D2MFS

(cavitated decayed, missing, and filled sur-

faces), D12MFS (non-cavitated, cavitated,

missing, and filled surfaces).

Statistical methods

A chi-square test was used to test the distri-

bution of subjects between groups for cate-

gorical independent variables. Mann–Whitney

U-tests were used to test the association

between dental caries as dependent variable

and independent variables. Multiple linear

regression analyses were performed to explore

the effect of independent variables on d12fs

and D12MFS as dependent variables. Children

were categorized according to frequency of

medicine application (1, 2 times ⁄day), spacer

use (no spacer, spacer), mouth rinsing after

medicine application (no mouth rinsing,

mouth rinsing), sugar content in medications

(non-sugar-containing and sugar-containing

medicines), length of medicine applications

(1–3, ‡4 years), consumption of food and

drinks (£5, >5times ⁄day), frequency of tooth-

brushing (1, 2, 3 times ⁄day), glucocorticoid

dose (50, 125, 250 lg), and parents’ educa-

tion (elementary school, vocational school,

secondary school, high school, university,

postgraduate studies).

The data were analysed using the SPSS

12.0 statistical software package for Windows

(SPSS Inc., Chicago, IL, USA). The level of

statistical significance was set at P £ 0.05.

Results

Weighted Cohen’s kappa values for intra-

examiner reproducibility were 0.87 (JJ) and

0.91 (TS), and for inter-examiner reproduc-

ibility, 0.81. The mean length of anti-asth-

matic medication use in 220 asthmatic

children was 4.7 ± 3.1 years. Thirty-five

(15.9%) asthmatic children used medicines

for 1 year, 159 (72.3%) used them from 2 up

to 8 years, and 26 (11.8%) from 9 up to

16 years. All asthmatic children used

glucocorticoid daily and bronchodilator as cir-

cumstances required. Of the asthmatic chil-

dren, 28 (12.7%) used additional leucotriene

antagonists and 5 (2.3%) used antihistamines.

Glucocorticoid in controlled-dose inhaled

form was used by 173 children (78.6%) and

in dry powder inhaled form by 35 (15.9%).

After medicine application, 180 (81.8%) asth-

matic children rinsed their mouths with

water. Inhalers with spacer were used by 168

(76.4%) children. Non-sugar-containing med-

ications were used by 157 (71.4%) children.

There was no statistically significant differ-

ence between the children with and without

asthma with respect to gender, fluoride

intake, dietary habits, oral hygiene, last den-

tal visit, and parents’ education (Table 2).

Asthmatic children aged 2–6 years had sig-

nificantly (P < 0.01) higher scores of d1, d2,

d2fs, and d12fs on their primary teeth

(Table 3), and significantly (P < 0.01) less car-

ies-free children than their non-asthmatic

counterparts. Asthmatic children aged

7–12 years had significantly (P < 0.01) higher

scores of d1, d2, d2fs, and d12fs on their pri-

mary teeth (Table 3), significantly (P < 0.01)

higher scores of D1, D2, F, D1MFS, D2MFS,

and D12MFS on their permanent teeth

(Table 4), and significantly (P < 0.01) less car-

ies-free children compared to the non-asth-

matic children in that age group. Asthmatic

children aged 13–17 years had significantly

(P < 0.05) higher scores of D1, D2, F, D1MFS,

D2MFS, and D12MFS when compared with

the non-asthmatic children (Table 4), the dif-

ference in the number of caries-free children

was not statistically significant (P = 0.071).

Multiple linear regression was used to

assess the influence of length, mode (i.e.,

spacer use, mouth rinsing with water after

medicine), and frequency of medicine appli-

cation, and its glucocorticoid dose and sugar

content on dental caries experience in perma-

nent teeth. The analysis was conducted in the

group of 125 asthmatic children, 7- to 17 years

old. They used glucocorticoid daily only via

controlled-dose inhaler; therefore, it was pos-

sible to assess the use of spacer in this group.

They used bronchodilator only in the acute

� 2012 John Wiley & Sons Ltd, BSPD and IAPD

Table 2. The study sample of asthmatic children and their controls with regard to gender, fluoride exposure history, dietaryhistory, oral hygiene, time since last dental visit, and parents’ education.

Asthmatic children Controls *P-value

Gender, n (%)Male 139 (63.2) 125 (56.8) 0.173Female 81 (36.8) 95 (43.2)

Fluoride exposure history, n (%)Use of fluoride pills 91 (41.4) 101 (45.9) 0.338Use of fluoride rinse or gel 40 (18.2) 47 (21.4) 0.402

Dietary history, n (%)Consuming food and drinks ‡5 times ⁄ day 133 (60.5) 128 (58.4) 0.668Drinking sweet drinks between meals 143 (65.0) 130 (59.4) 0.223Use of acid sport drinks 13 (5.9) 18 (8.2) 0.352Use of sweets 125 (56.8) 111 (50.5) 0.181Daily use of milk and cheese 162 (73.6) 166 (75.5) 0.662

Oral hygiene, n (%)Toothbrushing 1 time ⁄ day 41 (18.0) 36 (16.4) 0.530Toothbrushing 2 times ⁄ day or more 179 (81.4) 184 (83.6)

Last dental visit, n (%)In the last 6 months 178 (80.9) 178 (80.9) 1.000More than 6 months 42 (19.1) 42 (19.1)

Parents’ education, n (%)Elementary school 13 (5.9) 9 (4.1) 0.118Profession school 34 (15.5) 20 (9.1)Secondary school 89 (40.5) 80 (36.4)High school 22 (10.0) 29 (13.2)University 52 (23.6) 71 (32.3)Postgraduate studies 10 (4.5) 11 (5.0)

*P-value is from chi-square test.

Table 3. Mean ± SD number of decayed (d1-non-cavitated, d2-cavitated, d12-non-cavitated and cavitated) and filled (f)surfaces among asthmatic children and controls in primary teeth.

Age group n d1 ± SD d2 ± SD f ± SD d12fs ± SD

Asthmatic 2–6 60 2.50 ± 3.05** 9.98 ± 15.00** 2.43 ± 3.95 14.52 ± 14.90**7–12 141 0.57 ± 1.44** 5.09 ± 8.78** 2.99 ± 4.29 8.65 ± 10.49**

Controls 2–6 60 1.15 ± 1.97 2.82 ± 4.54 3.00 ± 4.89 6.97 ± 7.267–12 141 0.13 ± 0.53 0.84 ± 2.48 2.93 ± 3.79 3.90 ± 4.62

**P < 0.01, Mann–Whitney U-test.

Table 4. Mean ± SD number of decayed (D1-non-cavitated, D2-cavitated, D12-non-cavitated and cavitated), missing (M), andfilled (F) surfaces among asthmatic children and controls in permanent teeth.

Age group n D1 ± SD D2 ± SD M ± SD F ± SD D12MFS ± SD

Asthmatic 7–12 141 2.00 ± 2.85** 1.95 ± 2.58** 0 3.06 ± 4.11** 7.01 ± 5.59**13–17 19 5.16 ± 5.00* 8.53 ± 6.42** 0.63 ± 2.75 14.26 ± 9.55** 28.58 ± 12.71**

Controls 7–12 141 0.57 ± 1.32 0.13 ± 0.49 0 0.99 ± 2.15 1.69 ± 2.6313–17 19 2.05 ± 3.67 0.84 ± 1.07 0.32 ± 1.38 6.79 ± 6.49 10.00 ± 7.04

*P < 0.05, **P < 0.01, Mann–Whitney U-test.

Anti-asthmatic medications and dental caries 5

phase. We limited the age of the children to

those with permanent teeth only. In this

group, the influence of length, mode, and fre-

quency of medicine application, its glucocorti-

coid dose and sugar content on dental caries

� 2012 John Wiley & Sons Ltd, BSPD and IAPD

experience in permanent teeth was assessed.

The mean length of anti-asthmatic medication

use was 4.9 ± 2.8 years, with a maximum

length of 12 years. Inhalers with spacer were

used by 110 (88.0%) children. After medicine

6 T. Samec et al.

application, 103 (82.4%) children rinsed their

mouths with water, and 110 (88.0%) were

using non-sugar-containing medications. In

multivariate linear regression analysis, the

number of non-cavitated and cavitated caries,

missing, and filled surfaces (D12MFS) was the

dependent variable. The variance explained

by the model was 43%. Only the child’s age

was significantly (P = 0.00) associated with

caries experience of asthmatic children. High

glucocorticoid dose, increased frequency of

application, spacer use, and increased length

of medicine use were associated with high

D12MFS, but not statistically significant.

Mouth rinsing with water after medicine

application and sugar presence in medicines

was associated with low D12MFS, but not sta-

tistically significant.

To assess the influence of various con-

founding factors on caries experience in pri-

mary and permanent teeth in children of

different age groups, we utilized standard

multiple regression analysis (Table 5). Vari-

ables with P-values <0.20 in bivariate analysis

were selected for inclusion in a multivariate

model, as well as variables that previous stud-

ies had suggested were plausible predictors of

caries occurrence. The best models, based on

statistical significance for d12fs or D12MFS as

the dependent variable, were the models with

the following predictors: child age, asthma

diagnosis, parents’ education, consumption of

food and drinks ‡5 times ⁄day, daily glucocor-

ticoid dose, and frequency of toothbrushing.

In children aged 2–6 years, significantly

(P < 0.01) higher d12fs were found in children

with asthma diagnosis and of less educated

parents. In children aged 7–12 years, signifi-

cantly (P < 0.01) higher d12fs were found in

children of less educated parents and with

higher daily dose of glucocorticoid, and signifi-

cantly (P < 0.05) higher d12fs were found also

in children with asthma diagnosis and in

those who had consumed food and drinks

‡5 times ⁄ day. Higher D12MFS in children aged

7–12 years were significantly (P < 0.01) associ-

ated with asthma diagnosis and less-frequent

toothbrushing. In children aged 13–17 years,

only asthma diagnosis proved to be statistically

significantly (P < 0.01) associated with high

D12MFS in the model.

Discussion

In this study, the influence of exposure to

anti-asthmatic medications on the caries prev-

alence in children in Slovenia was investi-

gated. For the first time, it was shown that

asthmatic children have more non-cavitated

(i.e., ICDAS codes 1 and 2) as well as cavi-

tated lesions in their primary and permanent

teeth, and the proportion of caries-free chil-

dren was also smaller among the children

with asthma. The existence of non-cavitated

lesions, which were more prevalent than cav-

itated lesions, is an evidence of newly devel-

oping caries with chances of progressing to

cavitated caries, if an effective preventive

treatment is not implemented. These sug-

gested that there are factors that tilt the bio-

chemistry of the oral environment of

asthmatic children towards high caries risk,

indicating that asthmatic children are at a

high-caries-risk status.

The recognized importance of non-cavitated

primary lesions for caries risk assessment28

was ignored by previous studies, with few

exceptions, where also initial caries lesions

were recorded5,6,10,11,13,16,24. Inclusion of

early stages of the caries process improves the

precision of studies28. This trend was also

shown in the studies on adolescents and

young adults with asthma, where different

results were observed with initial and mani-

fested (frank) caries lesions; initial lesions

were significantly higher in patients with

asthma compared to the healthy controls,

whereas in manifested lesions, patients with

and without asthma had similar numbers10,11.

Asthmatic children had an increased preva-

lence of filled teeth surfaces on their perma-

nent teeth compared with controls, which is

an indication of a higher treatment need to

restore cavitated lesions. This observation is

consistent with the report of Kankaala et al.20

that asthmatic children receiving inhaled

glucocorticoids showed higher filling incre-

ments in the primary molars. Previous caries

prevalence studies showed that children in

younger age groups are more susceptible to

caries than older children29. Also, permanent

teeth were reported to be more at risk of car-

ies development30. In contrary, this study

� 2012 John Wiley & Sons Ltd, BSPD and IAPD

Table 5. Multiple regression analysis, on 440 children on primary teeth in 1 (2–6 years) and 2 (7–12 years) age group and onpermanent teeth in 2 and 3 (13–17 years) age group.

Independent variables B* SE† b‡ P-value

95% Confidenceinterval for B

Lower bound Upper bound

Model 1 (n = 120, age group: 2–6); dependent variable: d12fsConstant 11.04 4.98 0.029 1.17 20.91Child age (years) 1.47 0.89 0.14 0.101 )0.29 3.23Asthma 6.23 2.10 0.25 0.004 2.08 10.39Parents’s education )2.82 0.87 )0.29 0.002 )4.55 )1.10R2 = 0.18

Model 2 (n = 282, age group: 7–12); dependent variable: d12fsConstant 30.30 3.30 0.000 23.79 36.80Child age (years) )2.39 0.29 )0.42 0.000 )2.96 )1.82Asthma 2.38 1.08 0.14 0.028 )0.26 4.50Consuming food and drinks ‡5times ⁄ day 2.04 0.85 0.12 0.017 0.37 3.72Parents’s education )1.36 0.33 )0.21 0.000 )2.01 )0.71Daily glucocorticoid dose (lg) 0.01 0.01 0.18 0.004 0.01 0.02R2 = 0.32

Model 3 (n = 282, age group: 7–12); dependent variable: D12MFSConstant )2.83 1.94 0.145 )6.64 )0.98Child age (years) 0.76 0.15 0.22 0.000 0.43 1.09Asthma 5.22 0.50 0.51 0.000 4.24 6.20Frequency of toothbrushing )1.25 0.46 )0.13 0.007 )2.15 0.34R2 = 0.34

Model 4 (n = 38, age group: 13–17); dependent variable: D12MFSConstant )50.14 19.19 0.013 )89.09 )11.19Child age (years) 4.28 1.36 0.34 0.003 1.52 7.03Asthma 18.58 2.98 0.68 0.000 12.52 24.68R2 = 0.58

*B, unstandardized regression coefficient; †SE, standard error; ‡ b, standardized regression coefficient.

Anti-asthmatic medications and dental caries 7

showed that asthmatic children had signifi-

cantly higher caries prevalence in all age

groups in primary as well as in permanent

teeth. This is an indication that children with

asthma have some common factors predispos-

ing them to the risk of dental caries. This

study demonstrated these factors to include

the frequent and long-term exposure to

inhaled glucocorticoids, which was found to

be significantly associated with high caries

prevalence in both primary and permanent

teeth. This result is consistent with those of

Stensson et al.13, who found higher caries

experience in children with severe and very

severe asthma and doing regular use of

higher doses of glucocorticoids, compared to

those with mild and moderate asthma, who

would use glucocorticoids only periodically in

lower doses or not at all. Also, frequent use

of anti-asthmatic medications23 or the

increased severity of asthma22 was found to

be associated with increased caries experi-

ence. Previous studies also reported a dose–

� 2012 John Wiley & Sons Ltd, BSPD and IAPD

response effect of b2-agonists on impairment

of saliva secretion and composition14, adverse

effect of asthma severity on salivary flow

rate12, the correlation of the duration of med-

ication with decreased salivary pH and higher

salivary levels of Streptococcus mutans29, and

other important determinants that can influ-

ence caries process1.

The presence of lactose in some anti-asth-

matic medicines could, along with a

decreased salivary flow rate, promote the pro-

liferation of cariogenic bacteria18,22. In this

study, however, the association between lac-

tose-containing anti-asthmatic medications

and caries prevalence (D12MFS) was not sig-

nificant. This may be due to the sample size

where only 12% of the investigated children

were users of lactose-containing medications,

with some of them rinsing after medication

intake. In addition, although the proximal

surfaces were examined visually from the

buccal and lingual sides of the dentition, the

proximal caries, especially the incipient

8 T. Samec et al.

lesions, may have been underscored in this

study because of exclusion of bitewing radio-

graph from the examination. This is particu-

larly important because it has been predicted

that lactose in inhaler may lodge between the

teeth to cause caries in asthmatic children.

Bitewing radiograph as one of examination

methods was rejected by the ethics commit-

tee, who considers it an unnecessary expo-

sure of the children to ionizing radiation,

because there is no treatment component to

the study.

In this study, the use of spacer and rinsing

the mouth with water after medicine applica-

tion demonstrated to be protective factors in

caries development, although not statistically

significant. Spacer is believed to reduce the

amount of the lactose reaching the tooth sur-

face, whereas rinsing after medication intake

can facilitate cleansing away of residual sugar

from the tooth surfaces.

Asthmatic children did not differ signifi-

cantly from their non-asthmatic counterparts

with respect to gender, fluoride intake, die-

tary habits, oral hygiene, time since last den-

tal visit and parents’ education, although the

number of children consuming sweet drinks

between meals and consuming sweets was

higher in the group of asthmatic children,

which is in line with the results of Stensson

et al.16, where preschool children with asthma

showed higher intake of sugary drinks than

healthy controls. It was suggested that this

may be due to the dry mouth associated with

lower saliva secretion in asthmatic patients.

In this study, consumption of food and drinks

‡5 times ⁄ day proved to be a significant pre-

dictor in the model for the caries prevalence

in primary teeth as the dependent variable,

which confirms previous research16. Dental

caries lesions result from a shift in the ecol-

ogy and metabolic activity of the biofilm1,

which can be dramatically enhanced by add-

ing fermentable carbohydrates.

Parents’ education was associated with den-

tal caries prevalence in primary teeth,

whereas in permanent teeth caries prevalence

was influenced by frequency of toothbrush-

ing. This is in line with the observations of

previous studies31, showing that as the child

grows up, the influence of parents’ behavio-

ural factors gets smaller, and self-behaviour is

more important. In the study, we have not

considered variables such as mouth breathing,

saliva, or lifestyle in asthmatic children,

although these might also be potential con-

founding factors for dental caries.

The results of this study showed that chil-

dren with asthma who had used anti-asth-

matic medications had higher prevalence of

caries in primary and permanent teeth. This

calls for the development of an integrated

multidisciplinary oral health preventive pro-

gramme for these high-caries-risk population.

Further investigation is needed to elucidate

factors responsible for the association of anti-

asthmatic drugs with high caries prevalence.

Why this paper is important for paediatric

dentistsd This study shows that children with asthma that had

used anti-asthmatic medications had higher prevalence

of caries in primary and permanent teeth. The associa-

tion was observed with non-cavitated as well as with

cavitated caries lesions.d For these high-caries-risk children, an integrated mul-

tidisciplinary oral health preventive programme is

needed.

Acknowledgements

Supported by Slovenian Ministry of Science

and Education (No. P3-0374).

Conflict of interest

The authors declare no conflict of interest.

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