*University of Padova, Faculty of Medicine and Surgery, Department of PediatricDentistry

Via Ospedale Castelfranco Veneto, 31033 Treviso, Italy.**University of Padova, Faculty of Medicine and Surgery, Department of

PeriodontologyVia Venezia Padova, 35134, Italy

***Head of Dentistry Unit; Hospital of Cittadella (Padova), Italy

E-mail: gipsy_2k@hotmail.com

conditions with very complex aetiologies, variableclinical presentations and challenges in the diagnosisthat complicate attempts to study them.

Relatively few studies exist on oral health ofasthmatic patients. We find conflicting results in theprevious reports on the association between asthmaand oral disease [Hyyppä and Paunio, 1979;Bjekenbork et al., 1987; Storhaug, 1985; Kankaala,1998]. Findings, indicating an increased risk of oraldiseases in asthmatic patients are mainly obtainedfrom studies on children and adolescents. Accordingto most published reports, young asthmatic patientssuffer more from caries and/or periodontal diseasesthan non asthmatic subjects [Mc Derra et al., 1998;Ryberg et al., 1991; Arnup et al., 1993; Wierchola etal., 2006]. These findings were mainly obtained fromsmall scale studies. Shulman [Shulman, 2001] foundno association between dental caries and childhoodasthma, Meldrum [Meldrum, 2001] found no

IntroductionAsthma is one of the most common chronic diseases

in industrialised countries and its prevalence isconstantly increasing throughout the world [Haahtelaet al., 1990; Burney et al., 1990; Upton et al., 2000].Some of the studies report that the disease affectsapproximately 3-5% of the adult population and asmuch as 10% of children [Pearce et al., 2000].

Both asthma and dental caries are defined as chronic

Dental caries in children with asthmaundergoing treatment

with short-acting ß2-agonistsS. MAZZOLENI*, E. STELLINI**, E. CAVALERI*,

A. ANGELOVA VOLPONI**, R. FERRO***, S. FOCHESATO COLOMBANI*

ABSTRACT. Aim This study sought to evaluate possible higher risk for dental caries among asthmatic childrenundergoing treatment with short-acting ß2-agonists. Methods Dental clinical assessments, saliva analysis and aquestionnaire survey were carried out on 60 children aged 6-12, of whom 30 were asthmatic subjects undergoingtreatment with short-acting ß2-agonists and 30 were used as controls. The obtained data for DMFT/dmft scores,Silness-Löe plaque index, buffer capacity and bacteria counts for Streptococcus mutans and Lactobacillus in thesaliva, oral hygiene and dietary habits were compared using Student t-test and Pearson chi-square test. ResultsWe registered a higher DMFT score among asthmatics of 1.2±1.8 (SD) and 0.3 ± 0.8 among non-asthmaticpatients (p<0.05), while comparison of dmft scores between the examined groups showed not significant (Studentt-test). Saliva analysis revealed lower buffer capacity in 43.3% of the asthmatic children, followed by highercariogenic bacteria counts in their saliva (p<0.05 Student t-test). These results show the lower plaque index inthe asthmatic group (1.6 ± 0.4) compared with the control (2.1 ± 0.3). Asthmatic children expressed better oral-health habits with more frequent tooth-brushing and usage of fluorides. Conclusion The results from our studysuggest a higher caries-susceptibility among asthmatic children undergoing treatment with short-acting ß2-agonists, but a clear association between these drugs, salivary changes and dental caries among children, stillremains to be demonstrated.

KEYWORDS: Caries; Asthma; Short-acting ß2- agonists; Paediatric patients.

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association over time between asthma and cariesincrease and Eloot et al. found no dose-responserelationship between the severity and duration ofasthma and caries [Eloot et al., 2004].

Ryberg et al. [Ryberg et al., 1991; Ryberg, 1987;Ryberg et al., 1990] reported a link between increasedincidence of dental caries and regular use of inhaledß2-agonists used in the treatment of asthma. Thesestudies suggested that asthmatics may have alteredsalivary composition and flow rates due to thepresence of specific auto-antibodies to ß2-agonistsadrenergic receptors. These receptors are affected bythe administration of ß2-agonists anti-asthmatic drugs[Ryberg et al., 1991; Ryberg, 1991; Ryberg et al.,1990].

Other authors observed decreased salivary andplaque pH in asthmatic children who were usinginhalers [Kargul, 1998].

Taking into consideration the controversialconclusions found in the previous literature on apossible higher risk of dental caries among asthmaticchildren, we defined the objective of our study: toevaluate the prevalence of dental caries and gainfurther insight on dietary and hygiene habits amongchildren with asthma undergoing treatment with short-acting ß2-agonists.

Materials and methodsOur study population comprised 60 children aged 6-

12, of whom 30 (14 females and 16 males) wereasthmatic subjects, enrolled among the patientsvisiting the Paediatric Clinic of Pulmonary Diseases,University of Padua Hospital. All children werediagnosed with asthma, undergoing treatment withshort-acting ß2-agonists (salbutamol) in a form of oralinhalator, associated with a corticosteroid (fluticasonedipropionate), for at least 6 months beforeexamination.

The classification of diagnosed asthma was doneaccording to its severity [NHLBI/WHO, 1995].Duration of the treatment with short-acting ß2-agonists (salbutamol) was expressed in months.

All patients with diagnosed asthma who were notfollowing regular/continuous therapy (the minimumof six months before the examination), diagnosed withother pulmonary diseases or other health disturbances,treated with short-acting ß2-agonists or diagnosedwith lung diseases other than asthma, were excludedfrom the study.

The control group comprised 30 subjects (12females and 18 males) aged 6-12 enrolled amongpatients who came for regular check-ups at the

Clinical Department of Paediatric Dentistry,University of Padua. All subjects were clinicallyhealthy; none of them was under any medicaltreatment and had never been under treatment withß2-agonists.

To avoid bias of the saliva analysis, all subjects wereasked not to drink, eat, brush their teeth or eat chewinggums for at least one hour before examination.

All subjects that had been under antibiotic treatmentin the last two weeks before the examination wereexcluded from the study.

From the study, we excluded the patientsundergoing orthodontic treatment, fixed or removable,to avoid bias of the oral hygiene conditionsassessment.

Clinical assessmentOral examinations were carried out according to the

WHO guidelines [WHO, 1987]. The examinationswere performed in a dental chair, under a good lightusing a plane mouth mirror n. 5, and an explorer n. 23.The examinations were performed by one person in anblind manner.

The following data were registered.- DMFT/dmft - Decayed (D/d), missing or extracted

(M/e) and filled (F/f) teeth, for permanent anddeciduous teeth respectively.

- Measurement of the oral hygiene status by meansof the Silness-Löe plaque index [Silness and Löe,1964] based on recording both soft debris andmineralised deposits on the teeth.

- General condition of oral mucous membranes(cheeks and tongue) and lips.

Saliva analysisCollection and treatment of saliva samples were

performed using a standardised kit CRT IvoclarVivadent, composed by CRT Buffer e CRT Bacteria.

The CRT Buffer Test [CRT® Bacteria and BufferTest (Vivadent Ets., Lichtenstein)] was used todetermine the buffer capacity of saliva using acolorimetric test strip. The CRT Bacteria Testmeasured the Streptococcus mutans and Lactobacillicount in saliva by means of selective culture media.

Paraffin-stimulated whole saliva was collected incalibrated sterile tubes. CRT Buffer Test was strippedfrom the package without touching the yellow testfield. The entire yellow test field was wetted withsaliva using a pipette. To determine the buffer capacityof saliva, the color of the test field was compared withthe color samples after exactly 5 minutes of reactiontime. High, medium, and low salivary buffercapacities are indicated by blue, green, and yellow test

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134 EUROPEAN JOURNAL OF PAEDIATRIC DENTISTRY • VOL. 9/3-2008

fields, respectively. The saliva collected for the CRT Buffer Test was

also used for the CRT Bacteria Test. The agar carrierwas removed from the test vial, and a NaHCO3- tabletwas placed at the bottom of the vial. Using a pipette,both agar surfaces were wetted with saliva. The agarcarrier was placed back into the vial and closedtightly.

After incubation at 37°C for 48 hour, the density ofS. mutans and Lactobacilli colonies was assessedusing the corresponding evaluation pictures providedwith the kit. The presence of bacteria colonies over105 indicates a high risk for dental caries.

After obtaining an informed consent from each childand parent, according to the biomedical ethicsguidelines, the parent answered to a questionnairedealing with the following data:- background information (age, gender, place of

residence); - information on oral care habits (frequency of tooth

brushing and usage of fluoride tablets);- information on dietary habits (intake of sweets and

candies, soft and sweetened beverages).All patients included in the study came from the city

of Padua, Italy, that does not have community waterfluoridation.

Statistical proceduresComparisons between asthmatic children and

control group were made using the Pearson’s chi-square and Student t-test. The significance level wasset at p<0.05. All analysis was performed with SPSSfor Windows (version 12.0).

ResultsClinical findingsThe mean ± Standard Deviation (SD) age was 9±2.0

in asthmatic and 8.5±1.7 in non-asthmatic children. Weencountered different types of asthma among thechildren of the asthmatic group. Table 1 presents theclassification criteria for asthma categories with thenumber of subjects affected. Most of the subjectsaffected by asthma (80%) were undergoing treatmentfor a period between 6 and 12 months.

The statistical analysis revealed that there is asignificant difference in DMFT values between thetwo examined groups (asthmatic and control group),while the dmft values were not significantly different(Student t-test p<0.05). The mean Standard Deviation(SD) DMFT score was 1.2±1.8 in asthmatic and0.3±0.8 in non-asthmatic patients.

A significant difference was noted comparing the

plaque index between the two groups, where a lowerplaque index was registered among the asthmaticchildren.

Analysis of the salivaThe buffer capacity and bacteria load of the saliva

showed a significant difference in the two groups(p<0.05 Student t-test). For the asthmatic childrengroup the buffer capacity was notably lower and weregistered a low buffer capacity of the saliva in 43.3%

Classification and clinical features# n.

Mild Intermittent

Symptoms ≤ two times per week

Brief exacerbations (from few hours to few days)

Night times asthma symptoms, two times per month

Asymptomatic and normal lung functionbetween exacerbation

PEF o FEV1 ≥ 80% of predicted values; variability < 20%

Mild Persistent

Symptoms>two times per week, but <one time per day

Exacerbations that may affect activity

Night times asthma symptoms>two times per month

PEF o FEV1 ≥ 80% of predicted values;variability 20%–30%

Moderate persistent

Daily symptoms

Exacerbations that affect activity

Night times asthma symptoms>one time a week

Daily use of inhaled short-acting ß-agonists

PEF o FEV1 ≥ 60% e < 80% of predicted values;variability > 30%

Severe Persistent

Continuous symptoms

Frequent exacerbations

Frequent nighttimes symptoms

Limited physical activity

PEF o FEV1 < 60% of predicted values; variability > 30%

TABLE 1 - Classification of asthma by severity.Classification is based on the clinical features of asthmaticpatients. Sources: National Heart, Lung and Blood Institute.# Presence of one of the features of severity is sufficient toplace a patient in that category. A person should beassigned to the most severe grade in which any featureoccurs. FEV1 Forced expiratory volume in one second;PEF- Peak expiratory flow; n - Number of subjects.

2

13

13

2

of the asthmatic subjects (n=13), while no case of alow buffer capacity of the saliva was registered amongthe controls. Most of the non-asthmatic children 60%(n=16), expressed high buffer capacity of the saliva.

S. mutans and Lactobacilli counts showed as well asignificant difference between the two groups (Table 2).

Oral care and dietary habitsThe results of the questionnaire survey on the oral

care and dietary habits of the asthmatic and non-asthmatic children, brought to light a better oral careof the asthmatic children compared with the controlgroup. We noticed that 33.3% (n=10) of the asthmaticchildren brushed their teeth 3 times a day, whileamong controls only 6.7% (n=2) do so. Both of thegroups showed similar dietary habits and notsignificantly different.

DiscussionThe results from our study supported the hypothesis

that asthma may increase the risk of caries amongchildren undergoing treatment with short-acting ß2-agonists. We registered a higher DMFT score, lowerbuffer capacity and higher cariogenic bacteria countsin the saliva of the asthmatic children, in spite of theresults of better oral hygiene and lower plaque indexregistered among the asthmatic group compared withthe controls.

Our findings that the asthmatic children have higherDMFT scores than controls are in accordance with theresults reported by Milano [Milano, 1999]. Similar toour study, Milano’s study was conducted in a regionwhich does not have community fluoridation and hasless than 0.3 ppm natural fluoride (Texas Dpt. OfHealth 2000, for the city of San Antonio, US) [TexasDpt Of Health, 2000], as our study was conducted inthe region of the city of Padua that lacks communityfluoridation.

The different approach between our study and theone of Milano [Milano, 1999] lies in the fact that inthis study we included the subjects who were takingdietary fluoride supplements. Although moreasthmatic children were taking fluoride supplements,the difference between the two groups was notsignificant. On the other side, our findings differ fromthose reported by Kankaala [1998] and McDerra et al.[1998], who found significant differences in dfs anddft scores between asthmatics and controls. Kankaalaet al. [1998] found that asthmatic children had morerestorations and more extractions of primary molarsdue to caries than the controls. Our study showed nosignificant difference in the dmft scores among theexamined groups. A possible explanation for thedifference between our findings and those of McDerraet al. and Kankaala [Kankaala, 1998; McDerra etal.,1998] might be that most of the subjects included inour study were in the mixed dentition phase and the

TABLE 2 - Saliva analysis: Buffer capacity and density of S. mutans and Lactobacilli coloniesCRT® Bacteria and Buffer Test (Vivadent Ets., Lichtenstein).The CRT Buffer Test was used to determine the buffer capacity ofsaliva. High, medium, and low salivary buffer capacities are indicated. The density of Streptococcus mutans and Lactobacillicolonies was assessed using the corresponding evaluation pictures provided with the kit (CRT Bacteria Test). The presence ofbacteria colonies over 105 indicates a high risk for dental caries. Values with a superscript * in the table are significantlydifferent P < 0.05 (Student t-test). n - Number of cases; CFU - Colonies Formed Unit; SD - Standard Deviation; St Err –Standard Error.

Bacterial counts Buffer capacity of saliva

Streptoccoccus mutans Lactobacillus n

<105 <105 <105 <105 low medium high

CFU/L CFU/L CFU/L CFU/L

Asthmaticchildren 5 25 6 24 13 16 1

controls 24 6 27 3 0 12 18

SD 13.4 13.4 14.9 14.9 9.2 2.9 12.2

St Err 9.5 9.5 10.5 10.5 6.5 2.0 2.0

p >0.05* >0.05* >0.05* >0.05* >0.05* >0.05* >0.05*

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first molars were often decayed or filled. A possibledrawback of our study might be that the dental check-ups were performed in an unmasked manner, whichmay bias the results.

There are evident discrepancies in the previousreports on the prevalence of dental caries amongasthmatic children.

Recently, Shulman and Meldrum [Shulman, 2001;Meldrum, 2001] questioned the association betweencaries and asthma and our results clearly differ fromthose reported in their studies. The study design andapproach in time are as well different, taking intoconsideration that these studies are long-term studies

and included more subjects.The results of saliva analysis revealed lower buffer

capacity and an increased bacteria load in the saliva ofthe asthmatic children compared with the controlgroup. The alteration in the saliva buffer capacity andincrease of Streptococcus mutans and Lactobacillicounts in the saliva of the asthmatic childrenundergoing treatment with short-acting ß2-agonistscould be attributed to the diminished salivaryproduction and secretion associated to the prolongeduse of ß2-agonists, reported in some previous studies[Arnup et al., 1993]. The effect of reduced salivaryflow has been elucidated in both human and animal

TABLE 3 - Survey of oral care and dietary habitsResults from a questionnaire filled in by the parents of the examined children containing information on oral care habits(frequency of tooth brushing and usage of fluoride tablets) and dietary habits (intake of sweets and candies, soft and sweetenedbeverages). Values with a superscript * in the table are significantly different P < 0.05 (Student t-test). SD - Standard Deviation;St Err – Standard Error.

Asthmatic Controls SD St Err pchildren

Frequency oftooth brushing

Once/day 12 14 1.4 1.0 <0.05*

Twice/day 6 14 5.7 4.0 <0.05*

3 times/day 10 2 5.7 4.0 <0.05*

After each meal 2 - 1.4 1.0 <0.05*

Usage of fluoridetablets 1.4

Yes 20 16 2.8 2.0

No 10 14 2.8 2.0

Intake of sweetsand candies 1.0

3 times/day 29 29 0.0

5 times/day 1 1 0.0

10 times/day - - 0.0

>10 times/day - - 0.0

Intake of soft andsweetened beverages 0.6

3 times/day 27 24 2.1 1.5

5 times/day 3 6 2.1 1.5

10 times/day - - - -

>10 times/day - -

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studies [Ryberg et al., 1991; Arnup et al., 1993;Ryberg et al.,1988; Johansson and Ericson, 1987].Ryberg et al. [1987] demonstrated a reduction ofwhole and stimulated saliva of 26% and 36%respectively. Our results of lower buffer capacity of thesaliva and increase in cariogenic bacteria may be dueto the anti-asthmatic medications, containingfermentable carbohydrate and sugar, as suggested insome previous studies [Holbrook et al., 1989;Storhaug, 1985; Maguire et al., 1996; Tootla et al.,2005].

The inhaled drugs as salbutamol are delivered in acarrier powder which contains sugar. Some authorsshowed that almost all inhalant powders have a pHlower than 5.5 [O’Sullivan and Curzon, 1998].Lactose, that is commonly used as a carrier forsalbutamol sulphate,a is less cariogenic than othercommon sugars, but it has caries promoting potentialwhen associated with reduced salivary flow [Pearceand Sissons, 1987].

Since our analysis does not include the analysis ofsaliva flow, and certain chemical components, our dataare limited to the cariogenic bacteria counts and buffercapacity of the saliva, just as a possible indicator for ahigher caries-susceptibility.

However it remains to be demonstrated that there isa clear association between the suggested beta-agonists, salivary changes and dental caries amongchildren.

The data of our survey suggested that the asthmaticchildren, used to a continuous medical observation,follow the dental recommendations better and practicemore frequent tooth-brushing and usage of fluorides.

The two groups of children followed almostidentical dietary regime consuming sweets andsweetened beverages.

However this study shares the same problem asmany previous studies in children and adolescents,considering that the measurements were carried out onfairly small number of subjects.

ConclusionThe published reports give somewhat contradictory

picture on the association between asthma and dentalcaries.

The current study found supporting evidence for thehigher caries-susceptibility among asthmatic childrenundergoing treatment with short-acting ß2-agonists.We registered lower buffer capacity and highercariogenic bacterial load in the saliva of the asthmaticsubjects undergoing treatment. The results of higherDMFT scores, in spite of a lower plaque index and

better oral hygiene habits, can lead us to a conclusionthat the undergoing treatment with short-acting ß2-agonists may influence the caries-susceptibility amongthe asthmatic children. Nevertheless, the oralphysiological changes may be due to both disease andmedications and it remains very difficult to determinethe effects of the drugs and the disease itself.

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