Impact of oral health conditions on school performance and lost school days by children and adolescents: what are the actual pieces of evidence?

Aim: To investigate evidence of associations between oral health status of children and adolescents and their school performance and lost school days due to dental problems. Methods: PubMed electronic database was searched for scientific papers published between 1990 and 2013. Twenty-one papers that attempted to investigate the impact of oral health on school performance and lost school days were retrieved. Brief descriptions of each study’s methodology and outcomes were presented and discussed. Results: Although the papers reported statistically significant associations between school performance or lost school days and oral health conditions of schoolchildren, all of them were cross-sectional and ecological studies with an observational design, which may not provide full information about causes and effects. In addition, the lack of standardized criteria did not allow comparisons among the studies retrieved in the search. Conclusions: Oral diseases appear to impact on lost school days and school performance of children and policy-makers should address this issue when planning health promotion interventions in school settings. However, standardized materials and methodologies as well as longitudinal studies using valid and reliable criteria are needed to confirm the causes or risks of oral health factors in school performance, generating hypotheses for future research and providing important data for determining effective actions in school health programs.


Introduction
In 1948, the World Health Organization defined health as being "a state of complete physical, mental and social well-being, and not merely the absence of disease or infirmity" 1 .Oral health is considered an integral element of general health and well being because it enables individuals to eat, communicate and socialize with others 2 .Moreover, oral health is considered a mirror of general health and the mouth is a portal for infectious organisms to enter the whole organism 2 .Therefore, according to Sheiham 3 "the compartmentalization involved in viewing the mouth separately from the rest of the body must cease because oral health affects general health".
In spite of a range of oral diseases affecting the world's population, dental caries continues to be the most prevalent oral disease in children and adolescents worldwide, leading to pain, poor nutrition and time out of school, interfering in their quality of life [4][5][6] .Several studies have investigated the effect of chronic diseases 7 , such as asthma 8 , allergic rhinitis 9 , inflammatory demyelination of the central nervous system 10 and diabetes 11 on school performance.
In relation to oral health, Gift, et al. 12 (1992) showed that in 1989, over 51 million school hours were missed annually by North-American school-aged children as result of visits to dentists or oral problems.Moreover, according to the US General Accounting Offices 13 children with poor oral health are 12 times more likely to have restricted-activity days than those children without oral disease.
Although studies evaluating the impact of oral health conditions on school performance and lost school days are of growing concern to educational and health researchers, there remains an astounding lack of strict scientific inquiry that reviews the studies developed on this topic in order to ascertain the validity of the conclusions.
Considering the importance of this issue in planning health promotion activities in schools, the objectives of this study were to investigate the pieces of evidence and discuss the methods and results of studies that assessed the existence of associations between oral health status of children and adolescents, their school performance and lost school days due to dental problems.This evaluation aimed at providing researchers and decision makers with a more solid background needed to enlighten recommendations and interventions in the school settings.

Material and methods
The questions addresses by this review were "What evidence is there of an association between oral health and school performance?"and "What are the materials and methods used for studies about oral health and school performance?" For this purpose, an extensive literature search was carried out using Medline, ISI, Lilacs and Scielo databases.
The intent was to review all full-text papers published in biomedical journals between 1990 and 2013.The search strategy included the key words "school performance", "oral health" and "absenteeism".
The studies were screened according to the inclusion criteria: (1) research papers, (2) publications related to oral health, school performance and/or lost school days due to dental problems, (3) English-language papers.Studies conducted and published in other languages were excluded.
Two reviewers selected and reviewed the papers.First, each reviewer independently selected the papers after reading their abstracts and checking their contents.To validate the selection procedure, the reviewers examined the potentially relevant arguments against the inclusion criteria and all discrepancies were discussed until agreement was reached.

Results
The initial search retrieved 512 studies.One paper was excluded because it was duplicated.The titles and abstracts of the remaining 511 papers were reviewed for a more detailed evaluation.After review and discussion in situations of disagreement, only 17 papers met the inclusion criteria.The reasons for exclusion of the other papers are shown in Figure 1.
In a second round, a secondary search was conducted by investigating the reference list of the gathered literature and four more papers were included in the review due to the importance of the studies and strong relationship with the aim of this review 5,[14][15][16] .Table 1 shows the results of the studies.All papers included in this review were classified as having an observational clinical study design (cross-sectional studies and ecological studies).Table 1.

Results of references appraised
Impact of oral health conditions on school performance and lost school days by children and adolescents: what are the actual pieces of evidence?

Results of references appraised (cont.)
Impact of oral health conditions on school performance and lost school days by children and adolescents: what are the actual pieces of evidence?

Results of references appraised (cont.)
Impact of oral health conditions on school performance and lost school days by children and adolescents: what are the actual pieces of evidence?

Results of references appraised (cont.)
Impact of oral health conditions on school performance and lost school days by children and adolescents: what are the actual pieces of evidence?

Evaluation of school performance
With regard to data related to school performance in the review studies, they were generally obtained subjectively by questionnaires applied to parents 4,25 .For example, questions such as "in the last 12 months, how would you describe your child's performance in school" (excellent, above average, average, below average, or poor) were used in the study of Blumenshine et al. 4 (2008).Other studies used self-reports of children and adolescents as regards their school performance, ranked as low, moderate or high 21,[26][27] or even questions such as "In your opinion, what does your class teacher think about your school performance compared with that of your classmates?(good or poor)" '18 .Other studies, such as Freire et al. 19 (2008) used the question: 'Have you ever failed an examination at school?' and the responses were "no" and "yes" (failed once or more than once).
Instruments developed to assess the quality of life related to oral health (OHRQoL) such as the Oral impact on daily performance (OIDP) and Child Oral Impacts on Daily Performances (Child-OIDP) were also applied to students in some studies as an indirect means of obtaining their school performance 17,20,[28][29][30] .
In only three studies there were objective data about school performance obtained from standardized achievement tests.In the study by Muirhead and Locker 23 (2006), data were obtained from broad governmental educational research databases that used the criteria of the Education Quality and Accountability Office (EQAO) standard tests.Other indexes of academic performance were obtained from the Linguistic Awareness of Reading Readiness test of the emergent literacy test (LARR) 24 and Human Development Report 5 .The criteria used in EQAO were the percentages of grade three and grade six children scoring below the provincial average in reading, writing and mathematics 23 .In the LARR, school performance data included the results of baseline English, mathematics and literacy tests 22 .The study by Seirawan et al. 22 (2012) used The Los Angeles Unified School District (LAUSD) Office DATA and Accountability, which provide information about students' number of absent days, California Standards Test scores, proficiency levels.

Evaluation of lost school days
Another indirect way used in some of the reviewed studies to evaluate the school performance of schoolchildren was by quantifying the students' lost school days.Generally the studies used questionnaires applied to parents and schoolchildren to obtain these data 4,[14][15][16][31][32] .

Results of studies
All the evaluated studies showed associations among clinically detected (normative needs) and/or self-perceived oral health status (subjective needs) with school performance and school days lost by children and adolescents.

Discussion
To the best of our knowledge, this is the first study to review the quality of evidence related to the impact of oral health conditions on school performance and school days lost by children and adolescents.It was observed that all reviewed studies found statically significant associations between school performance or lost school days and the oral health conditions of schoolchildren.However, due to several limiting methodological factors observed in the studies, the associations observed could be inaccurate, generating weak evidence.

Designs of the studies
As regard the research design characteristics of the reviewed studies, it was observed that all of them were crosssectional and ecological observational studies.Observational studies are fast and have lower cost than longitudinal ones, but these studies are unable to show the causality or risk factors related to outcomes 33 .
In spite of this, they can indicate associations that may exist and are therefore useful in generating hypotheses for future research, providing important data to determine effective actions in public health 34 .Thus, it is recommended that longitudinal studies be developed in the future to evaluate the relative risk of the oral conditions impacting on school performance and absence from school due to dental problems, generating stronger evidence.

Evaluation of oral health conditions
The researchers in the reviewed studies used diverse ways of obtaining clinical data on oral health, by means of objective clinical data or subjective reports.
Most of the studies evaluated the oral needs of participants by normative clinical evaluation, such as caries and periodontal indexes [14][15][17][18][19][20]22,24 . Direct inspction of the oral cavity through well-established indexes and criteria, usually collected in a standardized manner by trained personnel, could be considered a reliable and valid method for evaluating oral health conditions.
On the other hand, the analysis of oral health conditions from the perceptions of parents, teachers or students' selfreports, as observed in some studies, might have subjective interpretations that could generate a systematic error arising Impact of oral health conditions on school performance and lost school days by children and adolescents: what are the actual pieces of evidence?
Braz J Oral Sci.12(3):189-198 from inaccurate measurement of the outcomes of the studied variables [26][27][28][29]32 . Thu, it is recommended that oral health indexes be used by calibrated teams of researchers in future studies for more reliable associations.

Evaluation of school performance
With regard to school performance, no standardized manner of collecting and measuring was observed in the reviewed studies, hindering the replication of studies and comparison of the data.Only three ecological studies used standardized data obtained from a government source for evaluating children's school performance 5,[22][23][24] .Although measures of school performance based on standardized tests have received criticisms due to the largely uncontrolled bias that could interfere in the measurement of intelligence, leading to failure in accurately predicting academic performance, it is likely that a strict standardization of the criteria used in these studies could permit comparisons among them 35 .With this assumption, the national standard achievement tests have commonly been used in studies evaluating associations between chronic diseases and school performance 6,[36][37] .
Other studies obtained data about missed school days or school performance from the reports of the schoolchildren's parents or directly from the schoolchildren 4,25 .The acquisition of data related to children's school performance obtained from parents or from schoolchildren must be scrutinized for the probability of information bias, since their perception could be mediated by subjective variables and cannot match the reality, producing data that are not reliable for research purposes.
In addition, instruments such as OIDP and Child-OIDP were used in some studies as an indirect means of evaluating student school performance.These instruments were originally developed to assess the quality of life related to oral health and measure the impact of oral problems on performing the daily life activities of individuals.Considering that school performance is a part of daily activities, this could be considered an indirect criterion used in studies for evaluating this objective.However, they are not specific instruments or criteria for evaluating school performance, which could generate inaccurate measurements or measurement biases.
Mikaeloff et al. 10 (2010) used grade retention as another criterion for evaluating children´s school performance.However, the use of grade retention data for this purpose depends on the educational system and criteria adopted in each region or country, and do not allow comparison among studies.

Associations between oral health, school performance and lost school days
The reviewed studies showed associations between dental problems of children and their school performance.According to Pourat and Nicholson 38 (2012) missed school days due to dental problems may have implications for the school performance of children, since absences from school mean missed opportunities for learning and academic advancement, and have significant negative social and economic consequences.
It was also observed that the majority of studies investigating the school days lost due to dental problems did not investigate the specific oral problem related to absenteeism, such as pain, dental caries, orofacial trauma or other oral problems.Lack of this information is a limiting study factor because it does not allow determining the specific oral causes associated with poor school performance and prevents comparisons among the studies.

The influence of other variables on school performance
Analyzing the factors that may interfere with school performance, it is important to control the confounding variables, such as general or systemic health of schoolchildren.Blumenshine et al. 4 (2008) stated that children with poor oral and general health are more likely to have poor school performance.Thus, general health could function as a confounding variable for the relationship between oral health and school performance 4,39 .Other confounding variables were related to socio-environmental conditions of the children, such as low socioeconomic status and low education level of the family, which exert great influence on disturbed schooling, together with the burden of disease 10,40 .This represents a challenge to public health interventions, especially in some populations, such as immigrants and lowincome individuals in whom oral problems are more frequent and who cannot afford private treatment 32,38,41 .
Furthermore, other factors must be considered in the association with school performance, as studies have related this variable to perceptions of children's oral health-related quality of life [42][43] .These recent findings provide evidence of the relationship between social determinants, such as quality of life and environment, and school performance and school absenteeism.
From the results of the present review, it was observed a need for developing longitudinal studies to evaluate whether oral health is a risk factor for school absenteeism and school performance, in order to understand the actual influence of oral health conditions on an individual's school performance, using more accurate and reliable data.In addition, the use of multivariate statistics can be an important way to control the confounding factors in these analyses, such as general health, quality of life and socio-environmental conditions.
All the reviewed studies encountered associations between oral conditions and school performance of children and adolescents.However, the lack of longitudinal studies, standardized methodologies for comparisons of results and objective and standardized criteria for data collection on oral conditions, school performance and absenteeism, could make the current evidence on the association of oral conditions with low school performance and absence from school seem inconclusive or weak.The need for developing studies with a longitudinal design using more reliable and valid criteria is emphasized in order to assess the causality or risk of oral health factors impacting on school performance, generating hypotheses for future research and providing Impact of oral health conditions on school performance and lost school days by children and adolescents: what are the actual pieces of evidence?
Braz J Oral Sci.12(3):189-198 important data for determining effective actions in school health programs.
The outcomes of this study should be interpreted in the context of some limitations.The main objective was to collect important publications about school performance and oral health, though it was not included an appraisal of the quality of the papers selected in the systematic review.