Is Visual Pedagogy Effective in Improving Cooperation towards Oral Hygiene and Dental Care in Children with Autism Spectrum Disorder? A Systematic Review and Meta-Analysis

Visual pedagogy has emerged as a new approach in improving dental care in children with autism spectrum disorders (ASDs). This paper aimed to evaluate and assess the scientific evidence on the use of visual pedagogy in improving oral hygiene skills and cooperation during dental care in children with ASDs. The review protocol was registered on the PROSPERO Register (CRD42020183030). Prospective clinical studies, randomized trials, interruptive case series, before and after comparison studies, and cross-sectional studies following the PRISMA guideline were searched in PubMed, Embase, Scopus, and Google Scholar using ad hoc prepared search strings. The search identified 379 papers, of which 342 were excluded after title and abstract evaluation, and 37 full-text papers were analyzed. An additional four papers were added after consulting reference lists. Eighteen papers were disregarded; 23 were finally included, and their potential bias was assessed using ROB-2 and ROBINS-I tools. The wide heterogenicity of the studies included does not allow for conclusive evidence on the effectiveness of visual pedagogy in oral hygiene skills and dental care. Nevertheless, a significant and unilateral tendency of the overall outcomes was found, suggesting that visual pedagogy supports ASD children in improving both oral hygiene skills and cooperation during dental care.


Introduction
Autism spectrum disorders (ASDs) have progressively acquired more and more dignity and importance in the world health panorama, even in the dental field. Children with ASD are greatly challenged when facing new experiences, and the dental environment is of particular concern due to the presence of several noises, smells, and visual stimuli that might exacerbate fear and anxiety [1][2][3]. Concerns about dental care may lead parents to avoid regular dental examinations [4]. A good level of oral hygiene is quite difficult to maintain, since they often refuse brushing and flossing [5,6], increasing the risk of dental caries and gingivitis compared to children not affected by ASD. In addition to poor oral hygiene, a high frequency of sugary food and beverage consumption is frequently reported [6,7].
Behavioral management techniques derived from pediatric dentistry practice (desensitization, positive-negative reinforcement, tell-show-do) have been used to improve the ability of children with ASDs to receive dental treatment and oral healthcare [8,9]. This approach is the first attempt in a series of approaches to overcome undesirable behaviors during oral examinations and dental procedures. Behavioral management can be effective for some, but not for every patient. Many children with ASDs still require advanced behavioral guidance techniques, such as protective stabilization, oral sedation, and general anesthesia, to provide dental care [10]. Behavioral approaches are the most common treatment approaches for children with ASDs, and interventions often include the use of visual pedagogy. It is defined as the ability to recognize and understand ideas conveyed through visible actions or images [11], and it can be used to enable and/or increase specific skills of children [10]. The method involves the use of pictures/imagines either printed on paper or administered though digital tools, such as computers, smartphones, and tablets; such feasible interactive aids are becoming more and more utilized with special needs children. Among the different visual tools available, the Picture Exchange Communication System (PECS) is a frequently used augmentative communication system, in which picture cards are used to teach functional communication to non-verbal or limited speech children [12]. Visual pedagogy protocols foresee the use of sketches and/or videos to repetitively teach children how to perform tooth brushing and which steps they will encounter during oral examinations and preventive and/or restorative treatments. The core of visual pedagogy is that children with ASDs become familiar with the storytelling that they will remember when in the dental office. A high number of studies have already been carried out on this approach, proving this to be effective in reducing anxiety and increasing compliance [4,5,13].
The purpose of this paper is the evaluation and grading of the scientific evidence of the existing literature on the use of visual pedagogy as a strategy for improving oral hygiene skills in children with ASDs. The effect of visual pedagogy on children's cooperation during dental care was also assessed. A systematic review and meta-analysis were designed and carried out for this purpose.

Materials and Methods
This review follows the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guideline [13]. The review protocol was registered on the International Prospective Register of Systematic Reviews (PROSPERO) with registration number CRD42020183030. The question was structured and focused according to the PICO format (Population, Intervention, Comparison, and Outcome): Population: Children with autism spectrum disorders; Intervention: Effect of visual pedagogy; Comparison: Visual pedagogy vs. no treatment or outcomes measured before and after visual pedagogy administration; Outcome: Oral hygiene skills (primary outcome) and/or cooperation during dental care (secondary outcome).

Eligibility Criteria
The inclusion criteria were: Type of study: prospective clinical studies, randomized trials, interruptive case series, before and after comparison studies, cross-sectional studies; Publication languages: papers published in English, Italian, and French; Time of publication: no time restriction applied, last accessed on 23 July 2020; Type of tool used: PECS, images on paper, such as dental books, picture cards, drawings, and printed photos, or on digital supports, such as tablets, dental apps, and/or videos; Primary outcome: clinical indices of oral hygiene skills, such as the plaque index (PI) and the gingival index (GI). Tooth brushing performance was also considered. Secondary outcome: indices of patient's cooperation level during dental procedures, such as the Frankl Behavior Score and the Likert Anxiety Scale, and/or the number of steps/procedures completed and time spent, measured by a dentist or a dental hygienist and/or a psychologist/educator.

Study Selection
The output of the reference searches was uploaded into Excel software 16.16 (Microsoft, Redmond, WA, USA), and duplicates were excluded after comparing the results from the different research strategies. Four authors (A.B., S.C., C.S., and T.G.W.) independently examined all of the abstracts; papers meeting the inclusion criteria were obtained in the full-text format. The authors independently assessed the papers to establish whether each paper should or should not be included in the systematic review. Disagreements were resolved through discussion and/or by full-text analysis in doubtful cases. Where resolution was not possible, another author was consulted (M.G.C.).

Data Collection, Summary Measures, and Synthesis of Results
Data collection and synthesis were independently carried out by four authors (T.G.W., A.B., C.S., and S.C.) using an ad hoc designed data extraction form (Table S1 extraction form), without masking the name of the journal, title, or authors. Studies selected were divided into two groups according to their primary outcome. In the first group, articles that investigated the effectiveness of visual pedagogy in improving oral hygiene skills in children with ASDs were included [14][15][16][17][18][19][20][21][22]. In the second group, articles that investigated the effectiveness of visual pedagogy in improving the patient's cooperation during dental care were included [4,[23][24][25][26][27][28][29][30][31][32][33][34][35]. To facilitate the synthesis, the results were summarized in tables. For each paper, these data were searched and recorded when available: (a) source, publication year, location, and study duration; (b) details/characteristics of the participants; (c) level of disability/verbal fluency; (d) type of tool used and visual pedagogy protocol and adjunctive tool when used.

Quality Assessment and Scientific Evidence
The risk of bias assessment was performed by three authors (M.G.C., A.B., and S.C.), and the Cochrane Risk of Bias tools for randomized and non-randomized studies were used for methodological quality evaluation. A per-protocol analysis was conducted with the aim of assessing the effect of starting and adhering to the intervention. The Cochrane collaboration's ROB-2 tool was used to assess the risk of bias for randomized studies [36]. The Excel (Microsoft Corporation, Washington, U.S.) tool for ROB-2 was used to input answers given to signaling questions, and then an algorithm estimated the overall risk of the bias according to the results for each domain as: low risk, some concerns, or high risk. The risk of bias plots were drawn using the Cochrane robvis web app [37]. The Cochrane collaboration's ROBINS-I tool was used to assess the risk of bias for non-randomized studies of intervention (NRSI) [38]. Authors answered signaling questions in each domain, and then estimated the overall risk of the bias according to the results for each domain as: low, moderate, serious, or critical.
A list of criteria was agreed upon by three authors (M.G.C., A.B., and S.C.) to be followed in bias assessment for both RCT and NRSI. The standardization of the research protocol was considered challenging, and it was not considered in a strict manner due to the need to frequently adopt individual, case-based strategies in approaching patients with ASDs [25]. A list of confounding domains and co-interventions was agreed upon, and they were identified as: type and severity of ASD; age; previous use of visual pedagogy; and the presence of a control group. Bias related to deviation from treatment protocol was rated as low if visual pedagogy was administered by health personnel, as moderate if it was administered at home and compliance was verified, and as serious/critical if visual pedagogy was provided at home and cooperation was not verified. The presence of drop-outs was of particular interest both in randomized and non-randomized studies, since no intention-to-treat analysis (ITT) was performed in any study. Drop-outs were judged as follows: drop-outs less than 10%, low risk; drop-outs of 10-20%, moderate risk; drop-outs of 20-30%, serious risk; drop-outs more than 30%, critical risk. Blinding is more often difficult in such studies, and was rated as follows: double blinding, low risk; single blinding, moderate risk; no blinding, serious risk. The risk of bias assessment was evaluated independently by three reviewers (A.B., S.C., and T.G.W) and then discussed together with a third reviewer (M.G.C.) in order to resolve disagreements and provide the overall final judgment for each study.

Statistical Analysis
STATA16 Software (Statacorp, College Station, TX, USA) was used for the metaanalysis of the data. The mean difference (MD) and odds ratio (OR) were chosen to calculate the effect size. The analysis was computed on the different visual tools used. A meta-analysis was performed if two or more studies compared the effect of visual pedagogy using comparable outcomes (G.C.). The I2 statistic was calculated to describe the percentage of variation across studies due to heterogeneity rather than chance [39]. The heterogeneity was categorized as follows: <30%, not significant; 30-50%, moderate; 51-75%, substantial, and 76-100%, considerable. Whether homogeneity was obtained or not, the random effects model (REM) with 95% confidence intervals was chosen as the meta-analysis model.

Study Selection
The search identified 478 papers; 379 were selected after removing duplicates, then 342 papers were excluded after a title and abstract evaluation (Table S2, List of excluded papers after the first evaluation). Thirty-seven papers were obtained in their full-text format, and an additional four papers were added after consulting the references lists ( Figure 1). Therefore, forty-one papers were assessed; eighteen papers were discarded (Table S3). Twenty-three studies were finally included in this systematic review: nine studies concerned tooth brushing and oral hygiene skills in children with ASDs and 14 studies concerned their cooperation during dental procedures ( Figure 1) [4,. The majority of the papers included (21 studies) were published in the last decade, with 10 papers published from 2018 to 2020 [14,16,17,19,[21][22][23]26,28,32] (Table 1).

Subjects Involved
An overall 1106 children with ASDs were included and evaluated, of which 532 were recruited for oral hygiene skills assessment and 574 for cooperation during dental treatment assessments after a visual pedagogy intervention. The patients' ages ranged from 3 to 23 years, with an overall minimum average age of 4.50 years and maximum of 12.28 years. Thirteen studies reported the intellectual disability level of the children involved [4,17,[20][21][22]24,[26][27][28][29][31][32][33].

Oral Hygiene Outcome
Oral hygiene skills improvement was assessed using two clinical outcomes: the Gingival Index (GI) and the Plaque Index (PI). Tooth brushing performance, as the number of subsequent steps acquired in a tooth brushing session, was also used ( Table 2).
Plaque index (PI) was measured in eight studies, six of which used the Silness and Löe Index [14][15][16][17][18]22], one study used the Podshadley and Haley Index [20], and one study used the Simplified Debris Index [21]. In four studies, the Gingival index (GI) was evaluated, three of which used the Löe and Silness Index [14,17,22], and one study used the Modified Gingival Index [21]. Tooth brushing performance was evaluated in two studies, where the tooth brushing session was split in five [18] and 13 [20] steps [19,21]. All studies included reported an improvement in tooth brushing performance and/or PI and GI indexes of ASD children after intervention with visual tools, and this was statistically significant (p < 0.05) in all [14,16,17,[19][20][21][22] except two studies [15,18].
The cooperation of children with ASDs during dental treatment was measured by the means of scores assigned according to the Frankl Behavior Scale in four studies [28,30,32,33], the Likert Anxiety Scale in one study [29], and the Venham Behavior Scale in one study [27].

Risk of Bias Assessment
Regarding the five RCTs (Figure 2), four were judged at a moderate risk of bias [9,23,27,31] and one at a high risk of bias [20]; among the 18 non-randomized studies (Table 4), one was judged at a low risk of bias [22], 16 were at a moderate risk of bias [4,[14][15][16][17][18][19]21,[24][25][26]28,30,32,33,35], and one was at a serious risk of bias [34]. Bias arising from the measurements of the outcomes significantly affected the quality rating of both the RCTs and the NRSIs. The randomization process aroused some concerns in more than 75% of RCTs (Figure 2), while confounding variables were not properly controlled in almost all NRSIs (Table 4).

Meta-Analysis
Data from four studies [14,15,17,22] were aggregated for meta-analysis, and a subgroup analysis by the type of tool was performed to assess the use of PECS and other types of visual tools (non-PECS) on Plaque Index results after six months (Figure 3).  The effect size was calculated within each group and across all studies using an inverse-variance model. Sub-group heterogeneity was moderate both in PECS (I 2 = 28.99%) and non-PECS (I 2 = 26.00%), while overall heterogeneity was high (I 2 = 81.32%). Both PECS and non-PECS aids were effective in PI improvements, but no differences were found between the two sub-groups (p = 0.34).

Discussion
Visual pedagogy has been proposed as an effective approach to allow children with ASDs to become familiar with a dental environment, help them cope during outpatient procedures, and learn oral hygiene skills to maintain good oral health status. This method is widely used at home and at school for daily life activities and educational purposes; it is based on the visual receptivity of pictures, photos, and videos, which enable communication in non-verbal and/or non-fluent patients, the learning of new activities or social cues, and a reduction of anxiety when dealing with unfamiliar situations [10].
The systematic review was designed and carried out to assess whether visual pedagogy is an effective tool for oral hygiene and outpatient dental care in children with ASDs.
Oral hygiene studies showed that visual pedagogy is effective in improving and maintaining good oral health in patients with ASDs, as revealed by improvement of PI and GI in all of the studies performing this evaluation. Almost all studies investigating behavior during dental care showed an increased cooperation of children. Overall, visual pedagogy is effective in improving oral hygiene/tooth brushing skills and cooperation levels in dental settings.
This method of dental management has been only recently investigated, as revealed by the small sample of eligible articles selected for this systematic review, mostly published in the last decade. Despite the few papers included in this systematic review, 1142 children with ASDs were evaluated, representing a good sample size to provide some considerations on this topic.
The risk of bias was present in all kinds of studies due to poor stratification and lack of homogeneous samples. The majority did not differentiate the ASD level, verbal fluency, and/or previous use of visual tools. Drop-out rates might be the consequence of involving patients who in any case would not be able to adequately comply to visual pedagogy, rather than a failure of the treatment itself. Patient selection and outcome measurements should be performed based on factors that can predict the patient's assignment to and/or performance in using visual tools to better outlying limits and indications of visual pedagogy in dental settings. A behavioral approach to dental care with children might be affected by an inner and unavoidable inter-operator variability that is difficult to reduce, even when treatment procedures are well-standardized [40].
Many NRSIs were single-arm studies, lacking a control group. It is important to perform such intervention studies in at least a double-arm design to avoid drawing inconsistent conclusions. Intervention studies on children with ASDs often struggle to have adequate blinding to overcome measurements bias. The reason is that these patients often require specialized dental teams working in environments dedicated to special needs children, where it is not always possible to have adequate personal staff.
The high heterogeneity of treatment protocols in studies evaluating the behavior of children with ASDs during dental treatment has made it difficult to compare results among different studies and not possible to develop a meta-analysis. Standardized visual pedagogy protocols should be planned by establishing a narrow range of both the frequency and types of visual tools used, with adequate validation of patients' and parents' cooperation by, for example, means of questionnaires. The majority of the studies evaluated cooperation during non-invasive and/or minimally invasive procedures; however, visual pedagogy needs to be evaluated also in invasive and/or more complex treatments, since its efficacy during oral check-ups has already been validated.
The meta-analysis performed on the four studies confirmed that visual supports are effective. The meta-analysis also addressed any differences between PECS and non-PECS visual supports: PECS revealed a slightly better performance, but no consistent conclusion can be drawn.

Conclusions
The wide heterogenicity of studies included in this systematic review does not allow for the conclusion of clear evidence on the effectiveness of visual pedagogy in dental settings. Nevertheless, its use improved both oral hygiene skills and cooperation during dental care in children with ASDs, even if it is not possible to clarify which visual tool is more effective.