Caries prevalence and socioeconomic factors in children with sickle cell anemia

The aim of the present study was to investigate caries prevalence and socioeconomic factors in children with sickle cell anemia. This study was conducted in 160 children with sickle cell anemia aged 3 to 12 years attending the Center for Hematology in Recife, Brazil. Data collection included interviews with guardians concerning social factors and oral examinations to determine the caries prevalence. Statistical analyses were performed using the Kruskal-Wallis and Pearson’s chi-square tests at a 5% significance level. The caries prevalence was 55.0%. The dmft index was 2.12, and the DMFT index was 1.50. Income significantly influenced dmft; the mean dmft was 4.57 in children whose family income was less than the Brazilian minimum wage (BMW), whereas in children with a family income three times the BMW or higher, the mean dmft was 2.27. No statistically positive association was found between the educational level of parents and guardians and the caries indices. A statistically significant association was found between dental caries prevalence and family income. Descriptors: Anemia, Sickle Cell; Oral Health; Dental Caries; Child; Socioeconomic Factors. Introduction Sickle cell anemia is a genetic disorder characterized by a mutant type of hemoglobin, called hemoglobin S (HbS), that causes the sickling of red blood cells.1 Sickle cell anemia is the most common hereditary disease in Brazil and worldwide.2-5 In Brazil, it is estimated that more than two million people carry the gene for HbS, and over 8,000 individuals have the severe form (SS). Approximately 700,000 new cases of sickle-cell disease occur annually.6 The disease is prevalent among African descendents.6,7 Sickle cell anemia, although treatable, is a chronic incurable disease involving medical, dental, genetic, and psychosocial factors.7,8 Dentists play an important role in preventing complications and improving the quality of life of patients with sickle cell disease9 because these patients are more susceptible to infections and periodontal disease.10 These patients are also at a higher risk of developing dental caries because of the high prevalence of dental opacities (changes in the formation and calcification of enamel and dentin), the frequent and continuous use of medication containing sucrose, and the high frequency of complications and hospitalization brought about by the absence of proper oral hygiene.11 Declaration of Interests: The authors certify that they have no commercial or associative interest that represents a conflict of interest in connection with the manuscript. Caries prevalence and socioeconomic factors in children with sickle cell anemia 44 Braz Oral Res. 2012 Jan-Feb;26(1):43-9 In the last two decades, there has been a marked decline in caries in Brazil and worldwide.12-14 Among the reasons for this are the addition of fluoride to toothpaste,15 changes in caries diagnoses,16 water fluoridation and improvements in socioeconomic conditions.12,14,15 The literature provides little information on various aspects of sickle cell disease. For example, few studies have examined the increased prevalence of caries in individuals with sickle cell disease.17-22 Given the peculiarities of sickle cell anemia and its sequelae in the oral cavity, this study examined caries and socioeconomic factors in children with this disease. Methodology This study was approved by the Ethics in Research Committee of the Center of Hematology of Pernambuco (HEMOPE) (number 036/2007). The investigation was designed as a cross-sectional study. This sample consisted of 160 patients with a clinical and laboratory diagnosis of sickle cell anemia treated at the HEMOPE in Recife, Brazil. The children were examined as they sought care at HEMOPE, and the inclusion criteria were subjects aged 3 to 12 years, which allowed intra-oral examinations, and consent of the parents or guardians to participate in the study. The exclusion criteria were other systemic diseases, psychiatric or neurological disorders, or other factors that precluded oral examinations. For the examination, we used medical records containing the odontogram to determine the dmft (number of decayed primary teeth, teeth extracted, and teeth that were filled) and DMFT (number of decayed permanent teeth, missing teeth, and teeth that were filled) indices in accordance with the World Health Organization (WHO) criteria.23 During the clinical examination, the examiner wore personal protective equipment (PPE) that met biosecurity standards and used a dental mirror and probe with a 0.5-mm ball tip and black-ring between 3.5 and 5.5 mm from the tip to determine the Community Periodontal Index (CPI). The interexaminer calibration consisted of a theoretical stage with the presentation of images and the criteria of the DMFT and dmft indices. A second stage was devoted to clinical practice, resulting in a Kappa of 0.825. Intraexaminer calibration consisted of reviewing one in every ten children, resulting in a Kappa of 0.85. Data on socioeconomic characteristics were collected through a previously validated form by the validation method of face with 20 parents or guardians, addressing questions about home address, gender, age, education level of parents or guardians and family income. Individuals interviewed in the validation were not included in the final sample. The Brazilian minimum wage (BMW) was considered in calculating family income, and subjects were classified into 3 groups: less than one BMW, one to two times the BMW and more than two times the BMW. Educational level was classified as follows: elementary, high school and college education. Data analyses were performed to obtain the following percentage measures and statistics: mean, median, and standard deviation. Kruskal-Wallis tests were used for comparisons. Pearson’s chisquare tests were used to evaluate associations between categorical variables and groups, including the odds ratio (OR) and confidence interval values for the measures. The margin of error used was 5.0%, and the intervals were obtained with a reliability of 95.0%. Data were entered into an Excel 2003 (Microsoft Corporation, USA) spreadsheet, and SPSS (Statistical Package for Social Sciences) version 13 (SPSS Inc., Chicago, USA) was used for all statistical calculations. Results This study included 160 children (42.5% boys and 57.5% girls). The response rate was 100% of all invited children; all subjects met the inclusion criteria. The mean dmft results showed that 78.7% of teeth were decayed, and 16.9% had been filled. The mean DMFT results for permanent teeth showed that 56% of the teeth were decayed, and 32% had been filled (Table 1). Over half (56.3%) of the parents and guardians had not completed their elementary education, Luna ACA, Rodrigues MJ, Menezes VA, Marques KMG, Santos FA 45 Braz Oral Res. 2012 Jan-Feb;26(1):43-9 18.1% had completed elementary school, and 18.1% had completed high school (Table 2). The income of the majority of families was one to two times the BMW, and only 15.0% earned a salary. There were no significant relationships between parental education levels and any of the examined variables (p > 0.05, Table 3). An examination of the influence of income on the average dmft and DMFT values (Table 4) revealed that decayed permanent teeth were more prevalent among those who had a family income of one to two times the BMW. The averages were correspondingly higher among children whose family income was less than the BMW. Income influenced dmft; the mean dmft was 4.57 in children whose family income was less than the BMW, whereas in children with a family income more than twice the BMW, the mean dmft was 2.27. However, the only significant differences between income categories occurred in the mean dmft (p < 0.05). As Table 5 shows, more than half (55.0%) of the sample had teeth with untreated caries. The prevalence of caries increased with age; caries prevalence was 36.0% among children 3 to 5 years old and 72.3% among those 9 to 12 years old. Caries prevalence was 6.6% higher in boys than in girls (58.8% versus 52.2%). Caries prevalence varied little between categories based on the education levels of parents and guardians. Caries prevalence was higher (62.5%) among children with family incomes below the Brazilian minimum wage compared with those who had incomes more than twice the BMW (50.0%). The only variable significantly associated with caries occurrence was age (p < 0.05). Discussion Although sickle cell anemia is the most common hematologic disease in Brazil,4 few studies have exVariable Statistics Mean Median SD Minimum Maximum Average (%)


Introduction
3][4][5] In Brazil, it is estimated that more than two million people carry the gene for HbS, and over 8,000 individuals have the severe form (SS). Approximately 700,000 new cases of sickle-cell disease occur annually. 6The disease is prevalent among African descendents. 6,7ickle cell anemia, although treatable, is a chronic incurable disease involving medical, dental, genetic, and psychosocial factors. 7,8Dentists play an important role in preventing complications and improving the quality of life of patients with sickle cell disease 9 because these patients are more susceptible to infections and periodontal disease. 10These patients are also at a higher risk of developing dental caries because of the high prevalence of dental opacities (changes in the formation and calcification of enamel and dentin), the frequent and continuous use of medication containing sucrose, and the high frequency of complications and hospitalization brought about by the absence of proper oral hygiene. 11raz Oral Res.2012 Jan-Feb;26(1):43-9 3][14] Among the reasons for this are the addition of fluoride to toothpaste, 15 changes in caries diagnoses, 16 water fluoridation and improvements in socioeconomic conditions. 12,14,15he literature provides little information on various aspects of sickle cell disease.][19][20][21][22] Given the peculiarities of sickle cell anemia and its sequelae in the oral cavity, this study examined caries and socioeconomic factors in children with this disease.

Methodology
This study was approved by the Ethics in Research Committee of the Center of Hematology of Pernambuco (HEMOPE) (number 036/2007).
The investigation was designed as a cross-sectional study.This sample consisted of 160 patients with a clinical and laboratory diagnosis of sickle cell anemia treated at the HEMOPE in Recife, Brazil.
The children were examined as they sought care at HEMOPE, and the inclusion criteria were subjects aged 3 to 12 years, which allowed intra-oral examinations, and consent of the parents or guardians to participate in the study.The exclusion criteria were other systemic diseases, psychiatric or neurological disorders, or other factors that precluded oral examinations.
For the examination, we used medical records containing the odontogram to determine the dmft (number of decayed primary teeth, teeth extracted, and teeth that were filled) and DMFT (number of decayed permanent teeth, missing teeth, and teeth that were filled) indices in accordance with the World Health Organization (WHO) criteria. 23During the clinical examination, the examiner wore personal protective equipment (PPE) that met biosecurity standards and used a dental mirror and probe with a 0.5-mm ball tip and black-ring between 3.5 and 5.5 mm from the tip to determine the Community Periodontal Index (CPI).
The interexaminer calibration consisted of a theoretical stage with the presentation of images and the criteria of the DMFT and dmft indices.A second stage was devoted to clinical practice, resulting in a Kappa of 0.825.Intraexaminer calibration consisted of reviewing one in every ten children, resulting in a Kappa of 0.85.
Data on socioeconomic characteristics were collected through a previously validated form by the validation method of face with 20 parents or guardians, addressing questions about home address, gender, age, education level of parents or guardians and family income.Individuals interviewed in the validation were not included in the final sample.The Brazilian minimum wage (BMW) was considered in calculating family income, and subjects were classified into 3 groups: less than one BMW, one to two times the BMW and more than two times the BMW.Educational level was classified as follows: elementary, high school and college education.
Data analyses were performed to obtain the following percentage measures and statistics: mean, median, and standard deviation.Kruskal-Wallis tests were used for comparisons.Pearson's chisquare tests were used to evaluate associations between categorical variables and groups, including the odds ratio (OR) and confidence interval values for the measures.The margin of error used was 5.0%, and the intervals were obtained with a reliability of 95.0%.
Data were entered into an Excel 2003 (Microsoft Corporation, USA) spreadsheet, and SPSS (Statistical Package for Social Sciences) version 13 (SPSS Inc., Chicago, USA) was used for all statistical calculations.

Results
This study included 160 children (42.5% boys and 57.5% girls).The response rate was 100% of all invited children; all subjects met the inclusion criteria.
The mean dmft results showed that 78.7% of teeth were decayed, and 16.9% had been filled.The mean DMFT results for permanent teeth showed that 56% of the teeth were decayed, and 32% had been filled (Table 1).
Over half (56.3%) of the parents and guardians had not completed their elementary education, 18.1% had completed elementary school, and 18.1% had completed high school (Table 2).The income of the majority of families was one to two times the BMW, and only 15.0% earned a salary.
There were no significant relationships between parental education levels and any of the examined variables (p > 0.05, Table 3).
An examination of the influence of income on the average dmft and DMFT values (Table 4) revealed that decayed permanent teeth were more prevalent among those who had a family income of one to two times the BMW.The averages were correspondingly higher among children whose family income was less than the BMW.Income influenced dmft; the mean dmft was 4.57 in children whose family income was less than the BMW, whereas in children with a family income more than twice the BMW, the mean dmft was 2.27.However, the only significant differences between income categories occurred in the mean dmft (p < 0.05).
As Table 5 shows, more than half (55.0%) of the sample had teeth with untreated caries.The prevalence of caries increased with age; caries prevalence was 36.0%among children 3 to 5 years old and 72.3% among those 9 to 12 years old.Caries prevalence was 6.6% higher in boys than in girls (58.8% versus 52.2%).Caries prevalence varied little between categories based on the education levels of parents and guardians.Caries prevalence was higher (62.5%) among children with family incomes below the Brazilian minimum wage compared with those who had incomes more than twice the BMW (50.0%).The only variable significantly associated with caries occurrence was age (p < 0.05).

Discussion
Although sickle cell anemia is the most common hematologic disease in Brazil, 4 few studies have ex- amined the oral health of children with this disease.These studies have observed an association between sickle cell anemia and dental caries, especially in children.However, these studies use different methodologies and samples, making it difficult to compare their results with the current results.
The main limitation of this study was that we examined a specific population and small number of cases.Therefore, the results should be interpreted cautiously, following the principles of special and external validity. 16We were forced to adopt this sampling model because of the difficulty in locating the study population.
Socioeconomic factors have been shown to influence caries risk. 24,25Low income may be associated with education levels and the value placed on health, lifestyle, and access to health care information.As a result, income may be an indirect factor for determining the susceptibility to dental caries. 25,26Laurence 21 found that poor Africans with sickle cell   anemia were at an increased risk of tooth decay.These results provide evidence that low-income individuals are more likely to have more decayed teeth compared with individuals without the disease.These results concur with our findings, in which the mean dmft was 4.57 and the mean DMFT 1.81 in children whose family incomes were less than the Brazilian minimum wage.In children from families with incomes more than twice the BMW, the mean dmft and DMFT were 2.27 and 0.30, respectively.Although education is the indicator most widely used to measure socioeconomic status in epidemiological studies, we did not find a significant positive association between the education level of the parents and guardians (Table 3) and the mean dmft or DMFT, unlike other research conducted in the same subject area. 27,28 a pilot study, Laurence et al. 19 found that patients with sickle cell anemia were more susceptible to dental caries than patients without the disease; the mean DMFT indices were 12.0 and 9.9, respectively.The results of the present study suggest that patients with sickle cell anemia are more susceptible to dental caries, although none of these differences was statistically significant.
The mean DMFT and dmft in our study were lower (DMFT = 1.50, dmft = 2.12) than those found by Laurence. 19However, this finding should be interpreted with caution, as the sample in the aforementioned pilot study included adults, limiting comparisons because of the wide age range involved (6 to 92 years).This older sample was likely associated with much higher caries rates.
The prevalence of untreated caries in our group was 55.0%, which was higher than the 22.95% prevalence found in a study of children aged 6 to 96 months in Bahia, Brazil. 17In Nigeria, Okafor 18 reported that the caries prevalence in individuals with sickle cell anemia was 35.13%, but they did not describe how they measured decay or how the statistical comparisons were made.One of the goals of WHO in relation to oral health for 2010 was to obtain DMFT scores ≤ 1.0 at 12 years of age. 29In our subjects, only the children aged 3-5 and 6-8 years attained the average recommended by WHO for 2010.
Although socioeconomic status is considered a risk factor for caries, 24,25 there are other biological, dietary and behavioral variables that were not considered in this study.These factors should be investigated in future studies.An important aspect to consider is that the prolonged use of drugs treating chronic diseases that are sweetened for children can cause harmful dental health effects, influencing caries activity. 4,30t is noteworthy that 45.0% of the children in the present study were free of caries.The implementation of health promotion strategies appropriate to children with sickle cell anemia is important to obtain significant reductions in dental caries.These strategies should result in children with good oral health, growth, and development, less morbidity and fewer episodes of pain, infections, and sickle cell crises.Oral health status can have a great impact on the overall health and life quality of people with sickle cell anemia. 11

Conclusions
As expected, our results, which showed a significant association between the prevalence of dental caries and socioeconomic factors, were similar to those reported by previous authors.This study found a high caries prevalence.There was a statistically significant difference between the mean dmft and family income; however no significant differences were found between the education level of parents and guardians and caries prevalence.

Table 2 -
Distribution of children examined according to the education level of their parents and guardians and family income.

Table 4 -
Mean and standard deviation for dmft and DMFTaccording to family income (Brazilian minimum wage).

Table 3 -
Mean and standard deviation of the dmft and DMFT averages according to the education of parents and guardians.

Table 5 -
Assessment of caries prevalence according to age, sex, and family income.