DOI: 10.1111/ipd.12111
An investigation into dental anxiety amongst paediatric cardiology patients AMY HOLLIS1, FIONA WILLCOXSON2, ADAM SMITH3 & RICHARD BALMER1 1
Department of Paediatric Dentistry, Leeds Dental Institute, Leeds, UK, 2Department of Paediatric Cardiology, Leeds Teaching Hospitals NHS Trust, Leeds, UK, and 3York Health Economics Consortium Limited, York, UK
International Journal of Paediatric Dentistry 2015; 25: 183–190 Background. There is evidence that children with
cardiac conditions have high levels of untreated dental disease. One possible explanation is that they are more dentally anxious as a result of increased exposure to medical interventions. Therefore, the primary aim of this study was to compare the level of dental anxiety between paediatric cardiology patients and healthy children. Methods. The study group comprised 54 children (mean age 12.2 years) who attended the outpatient paediatric cardiology clinic in tertiary care. The control group (n = 53, mean age 12.38 years) was recruited from consultant-led new-patient
Introduction
In spite of being high priority for dental care, studies consistently show that children with cardiac disease have dental caries levels that are at least as high as, if not higher than the general population1–5. In addition, high levels of untreated disease have been reported6–9 although most of the children in these studies had regular access to dental care. One possible barrier to the appropriate provision of dental care is the concept that children with chronic illness or a history of medical intervention are dentally more anxious and therefore more intolerant of dental treatment. Other potential patient-related barriers include a lack of dental awareness of the
Correspondence to: Amy Hollis, Department of Paediatric Dentistry, Leeds Dental Institute, Clarendon Way, Leeds LS2 9LU, UK. E-mail: [email protected] All authors have made substantive contribution to this study and/or manuscript, and all have reviewed the final paper.
orthodontic clinics. Child dental anxiety was measured using the Modified Child Dental Anxiety Scale (faces version). The parents completed the Modified Dental Anxiety Scale along with a questionnaire regarding their child’s medical and dental histories. Results. The mean level of dental anxiety was significantly higher in the study group (P < 0.05). Analysis of covariance indicated that overnight hospital admission history may have influenced the strength of this relationship. Conclusions. Paediatric cardiology patients had significantly increased levels of dental anxiety. It is likely that aspects of their medical history, notably overnight hospital admissions, are contributory factors.
patient and carer6, low dental attendance1 and dental health may be a low priority. In a case-control study of children referred to a specialist centre due to behaviour management problems10, 50% of the study group had a history of hospitalization compared to 29% of the controls. Many were found to have medical problems and were afraid of doctors’ visits. The authors linked these previous medical experiences to dental anxiety and their resultant behaviour management problems. Wright and Alpern11 similarly discovered an association between medical experiences, in particular painful experiences, and poor cooperation at the first dental visit. Colares and Richman12 also related previous hospitalization and health problems with behaviour in the dental setting. There are also studies specifically examining dental anxiety (not solely behaviour management problems) and its relationship to previous medical experiences. These are important as behaviour management problems are not necessarily synonymous with dental anxiety. Dentally anxious children can display positive behaviour in the dental environment.
© 2014 BSPD, IAPD and John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
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Children who have experienced frequent medical experiences have been shown to have increased dental anxiety13. Furthermore, those who have experienced unpleasant medical contacts are significantly more likely to have a high level of dental anxiety14–16. da Fonseca et al.1 discovered that parents of cardiac children believed their children became significantly more irritated and frustrated as a result of dental problems than the control group. However, no published research exists into the dental anxiety levels of paediatric cardiology patients. This is important to establish as dental anxiety cannot only have implications on behaviour management techniques but can also have a negative impact upon dental attendance17. Dentally anxious children can present with more behaviour management problems18, significantly higher levels of caries19–21 and have been shown to have a greater experience of dental general anaesthetics17. Such consequences can either complicate the dental management of paediatric cardiology patients or result in increased risk of morbidity and mortality for these children. Therefore, the primary aim of this study was to compare the level of dental anxiety amongst paediatric cardiology patients with a group of healthy children (ASA I). The secondary aims were to establish whether dental anxiety was affected by previous medical history in terms of number of overnight hospital admissions and number of general anaesthetics (GA) experienced. Methods
The acceptability of the materials and methods of this case-control study was informed by a pilot study which involved a convenience sample of 10 patients and parents attending for routine dental appointments. There were no major amendments after completion of the pilot study. Sample size was determined by using estimates from a previous study for the standard deviation22. Applying a power of 0.80 and significance level of 0.05, the final sample size after allowing 15% to enable the use of non-parametric tests and 10% for subject withdrawal was 53 for each group. Successive children attending the out-
patient paediatric cardiology clinic were recruited into the study group between October 2011 and February 2012. The control group consisted of healthy (ASA I) children who attended consultant-led new-patient orthodontic clinics between September 2011 and June 2012. Ethical approval was obtained from the National Research Ethics Committee Yorkshire and The Humber (East), UK (REC reference 11/YH/0191). Children were included in the study group if they were: 1) Between 8 and 16 years old with either structural or conductive cardiac defects; 2) Without any concomitant diseases or syndromes; and 3) Accompanied by an adult with parental responsibility for consent purposes. Potential participants were approached on the respective clinics by the investigator who provided information sheets before obtaining written consent from all parents and assent from all children who participated. Data collection took place in the waiting rooms of the clinics. The children completed the faces version of the Modified Child Dental Anxiety Scale (MCDASf), and their parents completed the Modified Dental Anxiety Scale (MDAS). Questions relating to the children’s medical histories in terms of cardiac diagnosis, number of previous general anaesthetics and experience of overnight hospital admissions were included in a questionnaire that the parents completed. Where parents were unsure of aspects of their child’s medical history, the medical notes were reviewed by the investigator and clarified by the cardiologist as needed. The children’s dental histories in terms of number of ‘fillings’, local anaesthetic (LA) injections, extractions under LA and extractions under GA were included in the questionnaire. Each child’s age, gender, and postcode were also recorded. The postcodes were used to allocate each participant to a deprivation quintile. The data were entered in to an electronic database and analysed using Statistical Package for Social Sciences (SPSS) software (version 19, IBM). Summary statistics were calculated to include frequencies, means, and standard deviations, where appropriate. The
© 2014 BSPD, IAPD and John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Dental anxiety amongst paediatric cardiology patients
differences in dental anxiety, medical experiences and dental experiences between the two groups were compared with the use of independent t-tests, Mann–Whitney U-test and chi-square tests. Within the study group, the mean level of dental anxiety was compared between children with conductive and structural defects. In addition, the severity of the cardiac diagnoses of children with structural cardiac defects was classified according to the complexity of the defect as simple congenital heart disease, moderate severity or great complexity23 to enable further subgroup analysis. Where significant differences were identified in the demographics and past experiences between the groups, further analysis was carried out using analysis of covariance (ANCOVA) to determine the potential effect that each of these variables had on the children’s dental anxiety scores. ANCOVA was used to statistically control for the significantly different covariates between the groups. Effect sizes were assessed using eta-squared (g2) for tests with a single predictor variable and partial eta-squared (g2p ) for those with multiple predictors. Eta-squared was interpreted as follows: 0.01 = small, 0.06 = medium, 0.13 = large effect size. For partial eta-squared (used for the ANCOVA) values >0.5 were interpreted as moderate and values >0.7 were interpreted as good effect sizes. The significance was set at P < 0.05. Results
The sample size of 106 was met. During the recruitment process five families declined to participate. Four of these were potential control participants. Fifty-four children were recruited into the study group and 53 children were recruited into the control group. There were no significant differences in the age (Mann–Whitney U = 1370.50, z = 0.38, P = 0.70) or gender (v2 ð1Þ = 2.13, P = 0.14) between the study and control groups. The mean ages were 12.20 years and 12.38 years, respectively, with a range of 8–16 years old in each group. The mean MCDASf score was 21.96 (SD 5.67) for the study group and 18.48 (SD 6.49) for the control group (Table 1). An independent t-test revealed that
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Table 1. Age and anxiety scores for study and control groups.
Age range Mean age Mean MCDASf Median MDAS Mean MDAS
Study group (n = 54)
Control group (n = 53)
8–16 years 12.20 years 21.96 (SD 5.67)* 11 (IQR 8–16) 12.83 (SD 5.95)
8–16 years 12.38 years 18.48 (SD 6.49)* 11 (IQR 8–16.50) 12.64 (SD 5.62)
*Significant difference according to an independent t-test (P = 0.004).
the mean level of dental anxiety in the study group was significantly higher than the mean level of dental anxiety for the control group (t (105) = 2.95, P = 0.004). The magnitude of the differences in the means (mean difference = 3.47, 95% CI: 1.14–5.81) was moderate (g2 = 0.08). There was no significant difference in the level of parental dental anxiety as measured by the MDAS between the groups (Mann–Whitney U = 1425.50, z = 0.03, P = 0.97). There was a significant difference in the deprivation quintiles between the two groups with the control group being significantly less deprived according to chi-square test (v2 ð4Þ = 17.44, P = 0.002). Therefore, the impact of the participants’ deprivation quintiles on the MCDASf scores between the two groups was determined using ANCOVA. After statistically adjusting for the difference in the deprivation quintiles, there was still a significant difference in the MCDASf scores between the two groups, with the study group being more anxious [F(1,94) = 8.78, P = 0.004, partial g2 = 0.09]. To identify any potential confounders relating to the participants’ dental histories, the dental experience in terms of LA, number of ‘fillings’, number of dental extractions under LA and exodontia experience between the study and control groups was compared. The only significant difference was that the study group had a significantly greater experience of extractions under GA (v2 ð1Þ = 4.14, P = 0.04). Therefore, an ANCOVA was conducted to investigate the impact of the children’s exodontia experience on the MCDASf scores between the two groups. After adjusting for the exodontia experience, there was still a
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significant difference in the MCDASf scores between the two groups with the study group being more anxious [F(1,104) = 8.40, P = 0.005, partial g2=0.08]. To investigate any potential impact the children’s medical histories might have had on dental anxiety, the number of overnight hospital admissions and GA experience between the groups was compared. Table 2 shows that the study group had experienced a significantly greater number of overnight hospital admissions (Mann–Whitney U = 528.00, z = 5.95, P = 0.001). The difference in the mean MCDASf scores was no longer significant when adjusting for the difference in overnight hospital admissions with ANCOVA [F(1,104) = 3.79, P = 0.054, partial g2=0.04]. The covariate of overnight hospital admissions, however, was not significant [F(1,104) = 2.36, P = 0.13, partial g2 = 0.02], suggesting that overnight admission history was unlikely to have had an effect upon the higher level of dental anxiety in the study group that is, this was not a strong relationship. Given that the difference in the level of child dental anxiety between the groups was no longer significant when adjusting for the difference in overnight hospital admissions, the relationship between child dental anxiety and overnight admission history in the study group was investigated further. There was a positive correlation between the MCDASf scores and the number of overnight admissions in the study group. The Pearson’s correlation coefficient revealed a weak, nonsignificant correlation between the two variables (r = 0.17, P = 0.21). This supports
the results of the ANCOVA in that overnight admissions were not an independent predictor of the level of dental anxiety in the study group. Although the difference in the number of general anaesthetics each group had experienced was significant (Mann–Whitney U = 528.00, z = 6.00, P = 0.001), as shown in table 3, there was still a significant difference in the mean MCDASf score between the groups when adjusting for the difference in the number of general anaesthetics the children in each group had experienced [F(1,104) = 4.34, P = 0.04, partial g2=0.04]. There was no relationship between the MCDASf scores and the children’s experience of GA [F(1,104) = 0.01, P = 0.92, g2=0.009]. Within the study group, there was no difference in the mean level of dental anxiety of children with structural cardiac defects when compared to those with conductive defects (Mann–Whitney U = 265.50, z = 0.78, P = 0.44). A one-way between-groups analysis of variance was conducted to explore the impact of cardiac complexity category on levels of dental anxiety. There was no significant difference in the MCDASf scores between children with simple (n = 13), moderate (n = 12), and great complexity (n = 9) congenital heart defects (F(2, 31) = 1.20, P = 0.31).
Table 2. Summary of overnight hospital admission history in the two groups.
Table 3. Summary of general anaesthetic history in the two groups.
Discussion
The main finding in this study was that the children with cardiac conditions were more dentally anxious than the control group. Furthermore, the mean MCDASf in the study
Overnight admission history
Group Study (n = 54) Control (n = 53)
General anaesthetic history
Mean
Median
Minimum
Maximum
3.06
2 (IQR 1–4)*
0
15
0.51
0 (IQR 0–1)*
0
4
n, number; IQR, interquartile range. *Significant difference according (P < 0.05).
to
Mann–Whitney
Group Study (n = 54) Control (n = 53) U-test
Mean
Median
Minimum
Maximum
1.87
1 (IQR 1–3)*
0
9
0.34
0 (IQR 0–1)*
0
3
n, number; IQR, interquartile range. *Significant difference according (P < 0.05).
to
Mann–Whitney
U-test
© 2014 BSPD, IAPD and John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Dental anxiety amongst paediatric cardiology patients
group (21.96) was higher than that for the normative data of the scale (19.81)22. Although analysis of deprivation revealed that there was a socioeconomic discrepancy between the groups, the difference in the level of dental anxiety between the two groups remained after accounting for this statistically. Therefore, socioeconomic background did not impact upon the level of child dental anxiety in the groups in this study. Both GA experience and number of overnight hospital admissions could be viewed as indicators of the degree of overall medical intervention the children had experienced and therefore, these factors were investigated. Both were significantly higher in the cardiac group. Further analysis of GA experience, however, demonstrated that (like socioeconomic status) the difference in the level of dental anxiety between the groups remained after statistically adjusting for this variable. It is possible that the increased GA experience in the study group could have been related to an increased level of dental anxiety resulting in the need for a dental GA. However, a longitudinal study design would have been needed to establish whether dental GA was required as a behaviour management tool or whether dental anxiety was a consequence of the use of GA. Furthermore, the use of a dental GA in the study group may have been employed to achieve optimal dental health in a timely manner and not necessarily due to a child’s dental anxiety. With regard to overnight hospital admissions, there was no longer a difference in the level of dental anxiety between the groups when the difference in admission experience was adjusted through the use of ANCOVA. Further analysis revealed a weak, non-significant correlation between the two variables. Therefore, the results indicated that overnight hospital admissions might influence a child’s level of dental anxiety. This is consistent with a much earlier study by Sermet16 who also identified a significantly greater number of hospital admissions amongst dentally anxious children compared with non-anxious children. Whilst it is possible that admission history has a greater sensitizing effect than the other variables investigated in this study, admission
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history did not solely explain the difference in the level of dental anxiety between the two groups. Indeed, Suprabha et al.24 did not identify any differences in the admission histories of children classed as having high dental fear using the Children’s Fear Survey Schedule Dental Subscale (CFSS-DS > 38) when compared to those with lower CFSS-DS scores. However, when a regression analysis was performed with dental fear as the dependent factor, hospital admission history appeared to contribute to dental fear. The authors concluded that past medical experiences were likely to influence dental fear but not behaviour. A study of the behaviour of children aged 3–6 years at a Brazilian University Dental Clinic reported a significant association between previous hospitalization and negative child behaviour12. It is possible that the more negative behaviour reflected a higher level of dental anxiety but this would have been difficult to determine in young children. The child’s temperament and lack of ability to cope with experiences such as hospital admissions may be important factors in children whom subsequently manifest dental anxiety. It is likely that other factors that were not identified in this study contributed to the aetiology of dental anxiety amongst paediatric cardiology patients. To identify specific predictors, further research into the nature of previous medical experiences in addition to subjective aspects such as the children’s response to such experiences is required. Ultimately the impact of any medical intervention on dental anxiety is more likely to be a result of the quality of each of the interventions (in terms of distress caused to the child) than the actual number experienced. The fact that the number of overnight hospital admissions had some impact on dental anxiety in this study may simply reflect that the chance of experiencing a traumatic admission increases with the overall number of admissions. This study, however, did not attempt to evaluate in any subjective way the quality of care in terms of distress caused to the child by previous medical or dental experiences but merely to control any potential confounding variables. Other factors that have previously
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been reported to impact upon child dental anxiety, for example, parental anxiety and gender were not shown to be significantly different between the groups in this study. There were some limitations which should be noted. The study and control groups consisted of convenience samples and therefore the samples may not have been truly representative. Children who failed to attend their appointments could have biased the sample as the reason for non-attendance could have related to higher anxiety levels in healthcare settings. However, due to the nature of the children’s diagnoses, it was likely that failure rates were minimal although these were not specifically recorded. Orthodontic patients were used as the control group as most patients attending were unlikely to have significant medical histories but would have had some experience of the dental environment. Previous studies involving paediatric cardiology patients have recruited controls from various samples such as children attending cardiology clinics as new patients who have been subsequently diagnosed with healthy hearts5, children from population registers4 and local schools3, siblings of children with cardiac defects2 and children attending dental outpatient clinics8. In this study, it was felt that children attending new-patient orthodontic clinics would offer the least bias sample. Although highly anxious children may be poor candidates for orthodontic treatment and therefore may not get referred for an orthodontic opinion, the new-patient orthodontic clinics were consultant-led clinics with specific referral criteria. Therefore, children attending these clinics were likely to have more complex orthodontic problems and children with severe orthodontic problems will get referred for an orthodontic opinion regardless of their dental anxiety. In addition to this, most patients should have been aware that their new-patient consultation would only involve a dental examination and radiographs where indicated and therefore, it was anticipated that failed appointments due to dental anxiety were low. The accuracy of the information provided by the participants’ parents could not be guaranteed due to recall bias. In an attempt
to improve the accuracy of the data, where parents in the study group were unable to recall aspects of their child’s medical histories, the patient’s medical notes were reviewed. Six parents were unsure of their child’s GA and/or overnight admission history so these were counted from the medical notes. This method was felt to be more accurate than complete reliance on parental recall for these families. It was not possible to assess factual validity for all participants due to time and clinic pressures. With regard to the reporting of the children’s dental experiences, a more reliable assessment of the children’s dental experiences could have been made following a dental examination of each participant. For practical reasons, dental examinations were not performed. Furthermore, it was felt that the reliability of using indices such as the total number of primary and permanent diseased, missing and filled teeth (dmft or DMFT) when investigating dental experience is poor. By using such indices, information regarding the exact nature of the dental intervention, for example, whether LA was used for a restoration, is not obtained and therefore, there would still have been a reliance on the families’ memory. Within the index, the ‘decay’ component could be indicative of dental avoidance behaviour or may simply reflect variations in dentists’ treatment philosophy, especially where the restoration of primary teeth is concerned. Obtaining dental records for all participants was another potential method for assessing the children’s dental history but this method would have been heavily reliant on the quality of the dental records. It is accepted that vulnerability to complications such as infective endocarditis, risks of GA and bleeding make children with cardiac disease a high priority for dental care and prevention. This study has demonstrated that these children also tend to be more dentally anxious and may explain to some degree the levels of untreated disease found in other studies in spite of their high risk status. This is another reason for targeted prevention in this group and something all clinicians treating these children should be aware of.
© 2014 BSPD, IAPD and John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Dental anxiety amongst paediatric cardiology patients
Conclusions
1) The study group was significantly more dentally anxious than the control group. 2) There were only weak relationships between child dental anxiety and GA and overnight admission experience. 3) An ANCOVA using the different and statistically significant variables as covariates (deprivation quintiles, exodontia experience, overnight hospital admissions, and GA experience) suggested that overnight hospital admissions may influence the level of child dental anxiety in this study. Child dental anxiety was not affected by deprivation, GA history or exodontia experience.
5
6
7
8
9
10
Why this paper is important to paediatric dentists ● Paediatric cardiology patients may present with higher levels of dental anxiety. Considering the evidence that paediatric cardiology patients also have increased caries experience combined with the increased risk to these patients if they suffer dental disease, the authors suggest these patients should be managed by specialists in paediatric dentistry.
11
12
13
Acknowledgements
We would like to thank the orthodontic and paediatric cardiology clinics for their help and support during the recruitment process. Conflict of interest
14
15
The authors declare no conflict of interest. 16
References 1 da Fonseca MA, Evans M, Teske D, Thikkurissy S, Amini H. The impact of oral health on the quality of life of young patients with congenital cardiac disease. Cardiol Young 2009; 19: 252–256. 2 Hallett KB, Radford DJ, Seow WK. Oral health of children with congenital cardiac diseases: a controlled study. Pediatr Dent 1992; 14: 224–230. 3 Pollard MA, Curzon ME. Dental health and salivary Streptococcus mutants levels in a group of children with heart defects. Int J Paediatr Dent 1992; 2: 81–85. 4 Stecksen-Blicks C, Rydberg A, Nyman L, Asplund S, Svanberg C. Dental caries experience in children
17
18
19
20
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with congenital heart disease: a case-control study. Int J Paediatr Dent 2004; 14: 94–100. Tasioula V, Balmer R, Parsons J. Dental health and treatment in a group of children with congenital heart disease. Pediatr Dent 2008; 30: 323–328. Balmer R. Bu’Lock FA. The experiences with oral health and dental prevention of children with congenital heart disease. Cardiol Young 2003; 13: 439– 443. Berger EN. Attitudes and preventive dental health behaviour in children with congenital cardiac disease. Aust Dent J 1978; 23: 87–90. Franco E, Saunders CP, Roberts GJ, Suwanprasit A. Dental disease, caries related microflora and salivary IgA of children with severe congenital cardiac disease: an epidemiological and oral microbial survey. Pediatr Dent 1996; 18: 228–235. Jowett NI, Cabot LB. Patients with cardiac disease: considerations for the dental practitioner. Br Dent J 2000; 189: 297–302. Holst A, Schroder U, Ek L, Hallonsten A, Crossner C. Behaviour management problems in child dentistry. Frequency, therapy and prediction. Swed Dent J Suppl 1988; 54: 1–55. Wright GZ, Alpern GD. Variables influencing children’s cooperative behavior at the first dental visit. ASDC J Dent Child 1971; 38: 124–128. Colares V, Richman L. Factors associated with uncooperative behavior by Brazilian preschool children in the dental office. ASDC J Dent Child 2002; 69: 87– 91. Karjalainen S, Olak J, Soderling E, Pienihakkinen K, Simell O. Frequent exposure to invasive medical care in early childhood and operative dental treatment associated with dental apprehension of children at 9 years of age. Eur J Paediatr Dent 2003; 4: 186–190. Bailey PM, Talbot A. Taylor PP. A comparison of maternal anxiety levels with anxiety levels manifested in the child dental patient. ASDC J Dent Child 1973; 40: 277–284. Majstorovic M, Skrinjaric I, Glavina D, Szirovicza L. Factors predicting a child’s dental fear. Coll Antropol 2001; 25: 493–500. Sermet O. Emotional and medical factors in child dental anxiety. J Child Psychol Psychiatry 1974; 15: 313–321. Nuttall NM, Gilbert A, Morris J. Children’s dental anxiety in the United Kingdom in 2003. J Dent 2008; 36: 857–860. Klaassen MA, Veerkamp JS, Hoogstraten J. Changes in children’s dental fear: a longitudinal study. Eur Arch Paediatr Dent 2008; 9(Suppl 1): 29–35. Milsom KM, Tickle M, Humphris GM, Blinkhorn AS. The relationship between anxiety and dental treatment experience in 5-year-old children. Br Dent J 2003; 194: 503–506. Shaw O. Dental anxiety in children. Br Dent J 1975; 139: 134–139.
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21 Townend E, Dimigen G, Fung D. A clinical study of child dental anxiety. Behav Res Ther 2000; 38: 31– 46. 22 Howard KE, Freeman R. Reliability and validity of a faces version of the Modified Child Dental Anxiety Scale. Int J Paediatr Dent 2007; 17: 281– 288.
23 Warnes CA, Liberthson R, Danielson GK et al. Task force 1: the changing profile of congenital heart disease in adult life. J Am Coll Cardiol 2001; 37: 1170–1175. 24 Suprabha BS, Rao A, Choudhary S, Shenoy R. Child dental fear and behavior: the role of environmental factors in a hospital cohort. J Indian Soc Pedod Prev Dent 2011; 29: 95–101.
© 2014 BSPD, IAPD and John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
An investigation into dental anxiety amongst paediatric cardiology patients AMY HOLLIS1, FIONA WILLCOXSON2, ADAM SMITH3 & RICHARD BALMER1 1
Department of Paediatric Dentistry, Leeds Dental Institute, Leeds, UK, 2Department of Paediatric Cardiology, Leeds Teaching Hospitals NHS Trust, Leeds, UK, and 3York Health Economics Consortium Limited, York, UK
International Journal of Paediatric Dentistry 2015; 25: 183–190 Background. There is evidence that children with
cardiac conditions have high levels of untreated dental disease. One possible explanation is that they are more dentally anxious as a result of increased exposure to medical interventions. Therefore, the primary aim of this study was to compare the level of dental anxiety between paediatric cardiology patients and healthy children. Methods. The study group comprised 54 children (mean age 12.2 years) who attended the outpatient paediatric cardiology clinic in tertiary care. The control group (n = 53, mean age 12.38 years) was recruited from consultant-led new-patient
Introduction
In spite of being high priority for dental care, studies consistently show that children with cardiac disease have dental caries levels that are at least as high as, if not higher than the general population1–5. In addition, high levels of untreated disease have been reported6–9 although most of the children in these studies had regular access to dental care. One possible barrier to the appropriate provision of dental care is the concept that children with chronic illness or a history of medical intervention are dentally more anxious and therefore more intolerant of dental treatment. Other potential patient-related barriers include a lack of dental awareness of the
Correspondence to: Amy Hollis, Department of Paediatric Dentistry, Leeds Dental Institute, Clarendon Way, Leeds LS2 9LU, UK. E-mail: [email protected] All authors have made substantive contribution to this study and/or manuscript, and all have reviewed the final paper.
orthodontic clinics. Child dental anxiety was measured using the Modified Child Dental Anxiety Scale (faces version). The parents completed the Modified Dental Anxiety Scale along with a questionnaire regarding their child’s medical and dental histories. Results. The mean level of dental anxiety was significantly higher in the study group (P < 0.05). Analysis of covariance indicated that overnight hospital admission history may have influenced the strength of this relationship. Conclusions. Paediatric cardiology patients had significantly increased levels of dental anxiety. It is likely that aspects of their medical history, notably overnight hospital admissions, are contributory factors.
patient and carer6, low dental attendance1 and dental health may be a low priority. In a case-control study of children referred to a specialist centre due to behaviour management problems10, 50% of the study group had a history of hospitalization compared to 29% of the controls. Many were found to have medical problems and were afraid of doctors’ visits. The authors linked these previous medical experiences to dental anxiety and their resultant behaviour management problems. Wright and Alpern11 similarly discovered an association between medical experiences, in particular painful experiences, and poor cooperation at the first dental visit. Colares and Richman12 also related previous hospitalization and health problems with behaviour in the dental setting. There are also studies specifically examining dental anxiety (not solely behaviour management problems) and its relationship to previous medical experiences. These are important as behaviour management problems are not necessarily synonymous with dental anxiety. Dentally anxious children can display positive behaviour in the dental environment.
© 2014 BSPD, IAPD and John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
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Children who have experienced frequent medical experiences have been shown to have increased dental anxiety13. Furthermore, those who have experienced unpleasant medical contacts are significantly more likely to have a high level of dental anxiety14–16. da Fonseca et al.1 discovered that parents of cardiac children believed their children became significantly more irritated and frustrated as a result of dental problems than the control group. However, no published research exists into the dental anxiety levels of paediatric cardiology patients. This is important to establish as dental anxiety cannot only have implications on behaviour management techniques but can also have a negative impact upon dental attendance17. Dentally anxious children can present with more behaviour management problems18, significantly higher levels of caries19–21 and have been shown to have a greater experience of dental general anaesthetics17. Such consequences can either complicate the dental management of paediatric cardiology patients or result in increased risk of morbidity and mortality for these children. Therefore, the primary aim of this study was to compare the level of dental anxiety amongst paediatric cardiology patients with a group of healthy children (ASA I). The secondary aims were to establish whether dental anxiety was affected by previous medical history in terms of number of overnight hospital admissions and number of general anaesthetics (GA) experienced. Methods
The acceptability of the materials and methods of this case-control study was informed by a pilot study which involved a convenience sample of 10 patients and parents attending for routine dental appointments. There were no major amendments after completion of the pilot study. Sample size was determined by using estimates from a previous study for the standard deviation22. Applying a power of 0.80 and significance level of 0.05, the final sample size after allowing 15% to enable the use of non-parametric tests and 10% for subject withdrawal was 53 for each group. Successive children attending the out-
patient paediatric cardiology clinic were recruited into the study group between October 2011 and February 2012. The control group consisted of healthy (ASA I) children who attended consultant-led new-patient orthodontic clinics between September 2011 and June 2012. Ethical approval was obtained from the National Research Ethics Committee Yorkshire and The Humber (East), UK (REC reference 11/YH/0191). Children were included in the study group if they were: 1) Between 8 and 16 years old with either structural or conductive cardiac defects; 2) Without any concomitant diseases or syndromes; and 3) Accompanied by an adult with parental responsibility for consent purposes. Potential participants were approached on the respective clinics by the investigator who provided information sheets before obtaining written consent from all parents and assent from all children who participated. Data collection took place in the waiting rooms of the clinics. The children completed the faces version of the Modified Child Dental Anxiety Scale (MCDASf), and their parents completed the Modified Dental Anxiety Scale (MDAS). Questions relating to the children’s medical histories in terms of cardiac diagnosis, number of previous general anaesthetics and experience of overnight hospital admissions were included in a questionnaire that the parents completed. Where parents were unsure of aspects of their child’s medical history, the medical notes were reviewed by the investigator and clarified by the cardiologist as needed. The children’s dental histories in terms of number of ‘fillings’, local anaesthetic (LA) injections, extractions under LA and extractions under GA were included in the questionnaire. Each child’s age, gender, and postcode were also recorded. The postcodes were used to allocate each participant to a deprivation quintile. The data were entered in to an electronic database and analysed using Statistical Package for Social Sciences (SPSS) software (version 19, IBM). Summary statistics were calculated to include frequencies, means, and standard deviations, where appropriate. The
© 2014 BSPD, IAPD and John Wiley & Sons A/S. Published by John Wiley & Sons Ltd
Dental anxiety amongst paediatric cardiology patients
differences in dental anxiety, medical experiences and dental experiences between the two groups were compared with the use of independent t-tests, Mann–Whitney U-test and chi-square tests. Within the study group, the mean level of dental anxiety was compared between children with conductive and structural defects. In addition, the severity of the cardiac diagnoses of children with structural cardiac defects was classified according to the complexity of the defect as simple congenital heart disease, moderate severity or great complexity23 to enable further subgroup analysis. Where significant differences were identified in the demographics and past experiences between the groups, further analysis was carried out using analysis of covariance (ANCOVA) to determine the potential effect that each of these variables had on the children’s dental anxiety scores. ANCOVA was used to statistically control for the significantly different covariates between the groups. Effect sizes were assessed using eta-squared (g2) for tests with a single predictor variable and partial eta-squared (g2p ) for those with multiple predictors. Eta-squared was interpreted as follows: 0.01 = small, 0.06 = medium, 0.13 = large effect size. For partial eta-squared (used for the ANCOVA) values >0.5 were interpreted as moderate and values >0.7 were interpreted as good effect sizes. The significance was set at P < 0.05. Results
The sample size of 106 was met. During the recruitment process five families declined to participate. Four of these were potential control participants. Fifty-four children were recruited into the study group and 53 children were recruited into the control group. There were no significant differences in the age (Mann–Whitney U = 1370.50, z = 0.38, P = 0.70) or gender (v2 ð1Þ = 2.13, P = 0.14) between the study and control groups. The mean ages were 12.20 years and 12.38 years, respectively, with a range of 8–16 years old in each group. The mean MCDASf score was 21.96 (SD 5.67) for the study group and 18.48 (SD 6.49) for the control group (Table 1). An independent t-test revealed that
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Table 1. Age and anxiety scores for study and control groups.
Age range Mean age Mean MCDASf Median MDAS Mean MDAS
Study group (n = 54)
Control group (n = 53)
8–16 years 12.20 years 21.96 (SD 5.67)* 11 (IQR 8–16) 12.83 (SD 5.95)
8–16 years 12.38 years 18.48 (SD 6.49)* 11 (IQR 8–16.50) 12.64 (SD 5.62)
*Significant difference according to an independent t-test (P = 0.004).
the mean level of dental anxiety in the study group was significantly higher than the mean level of dental anxiety for the control group (t (105) = 2.95, P = 0.004). The magnitude of the differences in the means (mean difference = 3.47, 95% CI: 1.14–5.81) was moderate (g2 = 0.08). There was no significant difference in the level of parental dental anxiety as measured by the MDAS between the groups (Mann–Whitney U = 1425.50, z = 0.03, P = 0.97). There was a significant difference in the deprivation quintiles between the two groups with the control group being significantly less deprived according to chi-square test (v2 ð4Þ = 17.44, P = 0.002). Therefore, the impact of the participants’ deprivation quintiles on the MCDASf scores between the two groups was determined using ANCOVA. After statistically adjusting for the difference in the deprivation quintiles, there was still a significant difference in the MCDASf scores between the two groups, with the study group being more anxious [F(1,94) = 8.78, P = 0.004, partial g2 = 0.09]. To identify any potential confounders relating to the participants’ dental histories, the dental experience in terms of LA, number of ‘fillings’, number of dental extractions under LA and exodontia experience between the study and control groups was compared. The only significant difference was that the study group had a significantly greater experience of extractions under GA (v2 ð1Þ = 4.14, P = 0.04). Therefore, an ANCOVA was conducted to investigate the impact of the children’s exodontia experience on the MCDASf scores between the two groups. After adjusting for the exodontia experience, there was still a
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significant difference in the MCDASf scores between the two groups with the study group being more anxious [F(1,104) = 8.40, P = 0.005, partial g2=0.08]. To investigate any potential impact the children’s medical histories might have had on dental anxiety, the number of overnight hospital admissions and GA experience between the groups was compared. Table 2 shows that the study group had experienced a significantly greater number of overnight hospital admissions (Mann–Whitney U = 528.00, z = 5.95, P = 0.001). The difference in the mean MCDASf scores was no longer significant when adjusting for the difference in overnight hospital admissions with ANCOVA [F(1,104) = 3.79, P = 0.054, partial g2=0.04]. The covariate of overnight hospital admissions, however, was not significant [F(1,104) = 2.36, P = 0.13, partial g2 = 0.02], suggesting that overnight admission history was unlikely to have had an effect upon the higher level of dental anxiety in the study group that is, this was not a strong relationship. Given that the difference in the level of child dental anxiety between the groups was no longer significant when adjusting for the difference in overnight hospital admissions, the relationship between child dental anxiety and overnight admission history in the study group was investigated further. There was a positive correlation between the MCDASf scores and the number of overnight admissions in the study group. The Pearson’s correlation coefficient revealed a weak, nonsignificant correlation between the two variables (r = 0.17, P = 0.21). This supports
the results of the ANCOVA in that overnight admissions were not an independent predictor of the level of dental anxiety in the study group. Although the difference in the number of general anaesthetics each group had experienced was significant (Mann–Whitney U = 528.00, z = 6.00, P = 0.001), as shown in table 3, there was still a significant difference in the mean MCDASf score between the groups when adjusting for the difference in the number of general anaesthetics the children in each group had experienced [F(1,104) = 4.34, P = 0.04, partial g2=0.04]. There was no relationship between the MCDASf scores and the children’s experience of GA [F(1,104) = 0.01, P = 0.92, g2=0.009]. Within the study group, there was no difference in the mean level of dental anxiety of children with structural cardiac defects when compared to those with conductive defects (Mann–Whitney U = 265.50, z = 0.78, P = 0.44). A one-way between-groups analysis of variance was conducted to explore the impact of cardiac complexity category on levels of dental anxiety. There was no significant difference in the MCDASf scores between children with simple (n = 13), moderate (n = 12), and great complexity (n = 9) congenital heart defects (F(2, 31) = 1.20, P = 0.31).
Table 2. Summary of overnight hospital admission history in the two groups.
Table 3. Summary of general anaesthetic history in the two groups.
Discussion
The main finding in this study was that the children with cardiac conditions were more dentally anxious than the control group. Furthermore, the mean MCDASf in the study
Overnight admission history
Group Study (n = 54) Control (n = 53)
General anaesthetic history
Mean
Median
Minimum
Maximum
3.06
2 (IQR 1–4)*
0
15
0.51
0 (IQR 0–1)*
0
4
n, number; IQR, interquartile range. *Significant difference according (P < 0.05).
to
Mann–Whitney
Group Study (n = 54) Control (n = 53) U-test
Mean
Median
Minimum
Maximum
1.87
1 (IQR 1–3)*
0
9
0.34
0 (IQR 0–1)*
0
3
n, number; IQR, interquartile range. *Significant difference according (P < 0.05).
to
Mann–Whitney
U-test
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Dental anxiety amongst paediatric cardiology patients
group (21.96) was higher than that for the normative data of the scale (19.81)22. Although analysis of deprivation revealed that there was a socioeconomic discrepancy between the groups, the difference in the level of dental anxiety between the two groups remained after accounting for this statistically. Therefore, socioeconomic background did not impact upon the level of child dental anxiety in the groups in this study. Both GA experience and number of overnight hospital admissions could be viewed as indicators of the degree of overall medical intervention the children had experienced and therefore, these factors were investigated. Both were significantly higher in the cardiac group. Further analysis of GA experience, however, demonstrated that (like socioeconomic status) the difference in the level of dental anxiety between the groups remained after statistically adjusting for this variable. It is possible that the increased GA experience in the study group could have been related to an increased level of dental anxiety resulting in the need for a dental GA. However, a longitudinal study design would have been needed to establish whether dental GA was required as a behaviour management tool or whether dental anxiety was a consequence of the use of GA. Furthermore, the use of a dental GA in the study group may have been employed to achieve optimal dental health in a timely manner and not necessarily due to a child’s dental anxiety. With regard to overnight hospital admissions, there was no longer a difference in the level of dental anxiety between the groups when the difference in admission experience was adjusted through the use of ANCOVA. Further analysis revealed a weak, non-significant correlation between the two variables. Therefore, the results indicated that overnight hospital admissions might influence a child’s level of dental anxiety. This is consistent with a much earlier study by Sermet16 who also identified a significantly greater number of hospital admissions amongst dentally anxious children compared with non-anxious children. Whilst it is possible that admission history has a greater sensitizing effect than the other variables investigated in this study, admission
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history did not solely explain the difference in the level of dental anxiety between the two groups. Indeed, Suprabha et al.24 did not identify any differences in the admission histories of children classed as having high dental fear using the Children’s Fear Survey Schedule Dental Subscale (CFSS-DS > 38) when compared to those with lower CFSS-DS scores. However, when a regression analysis was performed with dental fear as the dependent factor, hospital admission history appeared to contribute to dental fear. The authors concluded that past medical experiences were likely to influence dental fear but not behaviour. A study of the behaviour of children aged 3–6 years at a Brazilian University Dental Clinic reported a significant association between previous hospitalization and negative child behaviour12. It is possible that the more negative behaviour reflected a higher level of dental anxiety but this would have been difficult to determine in young children. The child’s temperament and lack of ability to cope with experiences such as hospital admissions may be important factors in children whom subsequently manifest dental anxiety. It is likely that other factors that were not identified in this study contributed to the aetiology of dental anxiety amongst paediatric cardiology patients. To identify specific predictors, further research into the nature of previous medical experiences in addition to subjective aspects such as the children’s response to such experiences is required. Ultimately the impact of any medical intervention on dental anxiety is more likely to be a result of the quality of each of the interventions (in terms of distress caused to the child) than the actual number experienced. The fact that the number of overnight hospital admissions had some impact on dental anxiety in this study may simply reflect that the chance of experiencing a traumatic admission increases with the overall number of admissions. This study, however, did not attempt to evaluate in any subjective way the quality of care in terms of distress caused to the child by previous medical or dental experiences but merely to control any potential confounding variables. Other factors that have previously
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been reported to impact upon child dental anxiety, for example, parental anxiety and gender were not shown to be significantly different between the groups in this study. There were some limitations which should be noted. The study and control groups consisted of convenience samples and therefore the samples may not have been truly representative. Children who failed to attend their appointments could have biased the sample as the reason for non-attendance could have related to higher anxiety levels in healthcare settings. However, due to the nature of the children’s diagnoses, it was likely that failure rates were minimal although these were not specifically recorded. Orthodontic patients were used as the control group as most patients attending were unlikely to have significant medical histories but would have had some experience of the dental environment. Previous studies involving paediatric cardiology patients have recruited controls from various samples such as children attending cardiology clinics as new patients who have been subsequently diagnosed with healthy hearts5, children from population registers4 and local schools3, siblings of children with cardiac defects2 and children attending dental outpatient clinics8. In this study, it was felt that children attending new-patient orthodontic clinics would offer the least bias sample. Although highly anxious children may be poor candidates for orthodontic treatment and therefore may not get referred for an orthodontic opinion, the new-patient orthodontic clinics were consultant-led clinics with specific referral criteria. Therefore, children attending these clinics were likely to have more complex orthodontic problems and children with severe orthodontic problems will get referred for an orthodontic opinion regardless of their dental anxiety. In addition to this, most patients should have been aware that their new-patient consultation would only involve a dental examination and radiographs where indicated and therefore, it was anticipated that failed appointments due to dental anxiety were low. The accuracy of the information provided by the participants’ parents could not be guaranteed due to recall bias. In an attempt
to improve the accuracy of the data, where parents in the study group were unable to recall aspects of their child’s medical histories, the patient’s medical notes were reviewed. Six parents were unsure of their child’s GA and/or overnight admission history so these were counted from the medical notes. This method was felt to be more accurate than complete reliance on parental recall for these families. It was not possible to assess factual validity for all participants due to time and clinic pressures. With regard to the reporting of the children’s dental experiences, a more reliable assessment of the children’s dental experiences could have been made following a dental examination of each participant. For practical reasons, dental examinations were not performed. Furthermore, it was felt that the reliability of using indices such as the total number of primary and permanent diseased, missing and filled teeth (dmft or DMFT) when investigating dental experience is poor. By using such indices, information regarding the exact nature of the dental intervention, for example, whether LA was used for a restoration, is not obtained and therefore, there would still have been a reliance on the families’ memory. Within the index, the ‘decay’ component could be indicative of dental avoidance behaviour or may simply reflect variations in dentists’ treatment philosophy, especially where the restoration of primary teeth is concerned. Obtaining dental records for all participants was another potential method for assessing the children’s dental history but this method would have been heavily reliant on the quality of the dental records. It is accepted that vulnerability to complications such as infective endocarditis, risks of GA and bleeding make children with cardiac disease a high priority for dental care and prevention. This study has demonstrated that these children also tend to be more dentally anxious and may explain to some degree the levels of untreated disease found in other studies in spite of their high risk status. This is another reason for targeted prevention in this group and something all clinicians treating these children should be aware of.
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Dental anxiety amongst paediatric cardiology patients
Conclusions
1) The study group was significantly more dentally anxious than the control group. 2) There were only weak relationships between child dental anxiety and GA and overnight admission experience. 3) An ANCOVA using the different and statistically significant variables as covariates (deprivation quintiles, exodontia experience, overnight hospital admissions, and GA experience) suggested that overnight hospital admissions may influence the level of child dental anxiety in this study. Child dental anxiety was not affected by deprivation, GA history or exodontia experience.
5
6
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8
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10
Why this paper is important to paediatric dentists ● Paediatric cardiology patients may present with higher levels of dental anxiety. Considering the evidence that paediatric cardiology patients also have increased caries experience combined with the increased risk to these patients if they suffer dental disease, the authors suggest these patients should be managed by specialists in paediatric dentistry.
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13
Acknowledgements
We would like to thank the orthodontic and paediatric cardiology clinics for their help and support during the recruitment process. Conflict of interest
14
15
The authors declare no conflict of interest. 16
References 1 da Fonseca MA, Evans M, Teske D, Thikkurissy S, Amini H. The impact of oral health on the quality of life of young patients with congenital cardiac disease. Cardiol Young 2009; 19: 252–256. 2 Hallett KB, Radford DJ, Seow WK. Oral health of children with congenital cardiac diseases: a controlled study. Pediatr Dent 1992; 14: 224–230. 3 Pollard MA, Curzon ME. Dental health and salivary Streptococcus mutants levels in a group of children with heart defects. Int J Paediatr Dent 1992; 2: 81–85. 4 Stecksen-Blicks C, Rydberg A, Nyman L, Asplund S, Svanberg C. Dental caries experience in children
17
18
19
20
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with congenital heart disease: a case-control study. Int J Paediatr Dent 2004; 14: 94–100. Tasioula V, Balmer R, Parsons J. Dental health and treatment in a group of children with congenital heart disease. Pediatr Dent 2008; 30: 323–328. Balmer R. Bu’Lock FA. The experiences with oral health and dental prevention of children with congenital heart disease. Cardiol Young 2003; 13: 439– 443. Berger EN. Attitudes and preventive dental health behaviour in children with congenital cardiac disease. Aust Dent J 1978; 23: 87–90. Franco E, Saunders CP, Roberts GJ, Suwanprasit A. Dental disease, caries related microflora and salivary IgA of children with severe congenital cardiac disease: an epidemiological and oral microbial survey. Pediatr Dent 1996; 18: 228–235. Jowett NI, Cabot LB. Patients with cardiac disease: considerations for the dental practitioner. Br Dent J 2000; 189: 297–302. Holst A, Schroder U, Ek L, Hallonsten A, Crossner C. Behaviour management problems in child dentistry. Frequency, therapy and prediction. Swed Dent J Suppl 1988; 54: 1–55. Wright GZ, Alpern GD. Variables influencing children’s cooperative behavior at the first dental visit. ASDC J Dent Child 1971; 38: 124–128. Colares V, Richman L. Factors associated with uncooperative behavior by Brazilian preschool children in the dental office. ASDC J Dent Child 2002; 69: 87– 91. Karjalainen S, Olak J, Soderling E, Pienihakkinen K, Simell O. Frequent exposure to invasive medical care in early childhood and operative dental treatment associated with dental apprehension of children at 9 years of age. Eur J Paediatr Dent 2003; 4: 186–190. Bailey PM, Talbot A. Taylor PP. A comparison of maternal anxiety levels with anxiety levels manifested in the child dental patient. ASDC J Dent Child 1973; 40: 277–284. Majstorovic M, Skrinjaric I, Glavina D, Szirovicza L. Factors predicting a child’s dental fear. Coll Antropol 2001; 25: 493–500. Sermet O. Emotional and medical factors in child dental anxiety. J Child Psychol Psychiatry 1974; 15: 313–321. Nuttall NM, Gilbert A, Morris J. Children’s dental anxiety in the United Kingdom in 2003. J Dent 2008; 36: 857–860. Klaassen MA, Veerkamp JS, Hoogstraten J. Changes in children’s dental fear: a longitudinal study. Eur Arch Paediatr Dent 2008; 9(Suppl 1): 29–35. Milsom KM, Tickle M, Humphris GM, Blinkhorn AS. The relationship between anxiety and dental treatment experience in 5-year-old children. Br Dent J 2003; 194: 503–506. Shaw O. Dental anxiety in children. Br Dent J 1975; 139: 134–139.
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A. Hollis et al.
21 Townend E, Dimigen G, Fung D. A clinical study of child dental anxiety. Behav Res Ther 2000; 38: 31– 46. 22 Howard KE, Freeman R. Reliability and validity of a faces version of the Modified Child Dental Anxiety Scale. Int J Paediatr Dent 2007; 17: 281– 288.
23 Warnes CA, Liberthson R, Danielson GK et al. Task force 1: the changing profile of congenital heart disease in adult life. J Am Coll Cardiol 2001; 37: 1170–1175. 24 Suprabha BS, Rao A, Choudhary S, Shenoy R. Child dental fear and behavior: the role of environmental factors in a hospital cohort. J Indian Soc Pedod Prev Dent 2011; 29: 95–101.
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