988368

1. Introduction 
The behavioral disorder is known as a serious problem in children with autism, which is characterized by persistent deterioration in social interaction, communication delay or deviation, and stereotyped patterns of interaction [1, 2, 3]. This disease can be diagnosed among 18-24 months infants; however, a definitive diagnosis may be made until the age of three years old in children [4]. Epidemiological studies on the prevalence of autism showed that the prevalence of this disorder is increasing worldwide [5], in boys 1 per 42 cases and girls 1 per 189. Moreover, it affects boys 4.5 times more than girls [6, 7]. In Iran, based on the study by Samadi et al., the prevalence of autism spectrum disorder has been reported to be 6.26 per 10000 people [8]. This high prevalence will urge care-providing organizations to face many challenges in Iran in a little while [9]. Accordingly, the inability of these children to identify emotional states and subsequently to provide appropriate responses limits their communications with other people specialty with their families [10]. The impaired emotional perception consequently leads autistic children to pay less attention to faces [11]. So, during interactive status, these children cannot recognize people’s emotional situations such as enthusiasm, anxiety, fear, and sadness based on the face or speech tone [12, 13, 14, 15, 16]. Additionally, the inability to recognize the emotional states of other people leads to the rejection of children with autism by peers and consequently to the occurrence of their violent behaviors towards themselves and others [17, 18, 19]. While an important factor in good interaction is identifying one’s emotional state, it is obvious that the disability of autistic children drastically reduces their constructive interactions [20, 21]. In the last decade, some studies have examined the interactive problems of autistic children and the effect of education on their communication and stated that structured and accurate education can improve the communication of these children [22, 23]. In this way, Conallen et al. showed that teaching emotional states of the face improved communication in children with autism [24]. Hassanpour et al. also reported that education improved the recognition of the emotional states of the face in children with autism [25]. In addition, some studies showed that education can decrease communication problems in these children, which consequently improves their constructive communication with others [26, 27]. So, due to the intensification of children with autism in Iran (8000 children with autism) [22] and limited studies that were performed about the recognition of emotional states of the face by autistic children. This research was implemented to evaluate the effect of education on recognizing facial emotions in children with autism.

2. Materials and Methods
Research design
This research was a single-blind randomized clinical trial that was conducted from January 2019 to August 2020 in three autistic children centers related to the University in the west of Iran. This study was conducted based on the consolidated standards of reporting trials.

Sampling method and participants
Autistic children together with their mothers participated in the present study. Based on Conallen et al. study, the sample size was estimated at 27 participants for each group (β=0.80, α=0.05). The participants were selected by accessible sampling method, then they were allocated by random sampling method to the study groups (intervention and control). The inclusion criteria were as follows: children aged 6-12 years old, having moderate to the high performance of autism in accordance with the diagnostic and statistical manual of mental disorders, 5th edition (DSM-IV) and the doctor’s opinion, having the ability to comprehend education, lacking other physical, psychic, and mental diseases, having no optic disorder, having no shift in the sort and dose of drugs during a month ago, and having consent to participate in the present research. Also, the exclusion criteria were as follows: absence in three or more education sessions and changes in the amount of the drug in children. A total of 60 autistic children participated in this study, but 6 autistic children were excluded due to a shift in the sort and dose of drugs. Finally, 54 autistic children remained in the study and were randomly allocated to the study groups. Also, two mothers of autistic children were excluded from the intervention group due to being infected with COVID-19 and unwillingness to continue participation in the study (Figure 1).

Outcome measures
Demographic information
The information in this questionnaire included age, sex, financial status, number of children in each family, number of autistic children in each family, functional level of autism, parents’ age, parents’ education of parents, and jobs of the mother’s parents.

Benton visual recognition test
The Benton test was used for the evaluation of face recognition. This test evaluates cognitive diminution in children in school aged 6-12 years. This 28-item test included related emotional faces (happiness, sadness, fear, and anger). Each emotional face has 7 pictures that children must select the appropriate picture according to the question. The child needs 1 minute to answer each question. The score of this test is gained by the sum of correct answers [24]. Shiri et al. stated that this test had good validity and reliability of 98% [28].

Study intervention
The researcher trained the autistic children in ten 20-min sessions, once per week for 10 weeks in the presence of their mothers. Correspondingly, the mothers were present beside the researcher. Therefore, mothers learned how to educate their children. Forty images were used for training based on the status of happiness, sadness, anger, and fear and every emotional face condition had 10 pictures. The pictures were designed based on a study by Conallen et al. The face and content validity of these pictures was assessed by 10 faculty members with about 5 years of experience in teaching behavior to children with autism children. They chose the emotional face image that related to the target image. The researcher and the mother assist autistic children in selecting the correct image. An image of a boy in A5 size and color was used for all images. The images were displayed to each child, and without explanation, autistic children must choose the image that matched the target image. When the child correctly identified one picture, the mother or researcher encouraged the child, and in the following, the next image was taught. But if the child was incorrect, a small and indirect guide was given to the child, and was asked to answer with more attention. If the child repeated the wrong answer, the child directly referred to the correct answer, and until the time the participant recognized the answer correctly, the process was repeated. In each session, the child received teachings with four pictures (each picture for an emotional state). The mother was present beside the researcher when mothers learned teaching to the child and had the desire and readiness to teach the child, the researcher would entrust the teaching of one or more images to the child and would supervise the child’s education by the mother, so education was done correctly. Meantime, the researcher explained more if mothers had ambiguities and questions about the images taught in each session. Parents of children with autism in the control group received routine training. The assistant researcher collected questionnaires in both groups one day before, one and seven days after the study, and was not informed of the allocation of children into two groups.

Statistical analysis
The obtained data were analyzed with the SPSS software, version 22. In this study, the Kolmogorov-Smirnov test confirmed the normal distribution of data. To compare demographic information between the two groups, we used the independent t test, Fisher exact, and Chi-square test. Also, to compare the two groups at the three time points, we used a repeated measures test. P values less than 0.05 were considered statistically significant.

3. Results
The majority of autistic children (33, 62.96%) were boys, and more children were in the medium functional level of autism. The Mean±SD ages of autistic children were 11.24±2.14 and 11.54±2.91 years in the control and intervention groups, respectively.
Most mothers of children with autism (15, 27.77%) had a secondary school level of education and were self-employed (22, 40.74%). The average ± SD ages of the mothers of children were 381.14±1.32 and 38.42±1.24 years in the control and intervention groups, respectively. Thus, the two groups were homogeneous (P>0.05) (Table 1).


The facial recognition scores were low in both groups in the pretest, especially identifying anger status (Table 2).

Therefore, no statistically significant difference was found in emotional facial scores at the beginning of the study between the intervention and control groups (P=0.93). However, after performing education, there was a statistically significant difference between both groups in the post-test (one day and seven days later) (P<0.001). In addition, there was a statistically significant difference in each group at three time points (P=0.025) (Table 3).

4. Discussion
The prevalence and spread of autism in the world and especially in Iran, have led care systems, families, and especially parents to face many challenges in educating and interacting with children with autism [25]. Therefore, the present study was conducted regarding the shortcomings of the educational program offered to children with autism in Hamedan City, Iran, to investigate the effect of education on facial emotions on improving the identification of facial emotion states in these children. The majority of the children included in this study were boys in the age range of 8-10 years with moderate functional levels. In other studies, the majority of infants were boys, but these studies have generally evaluated a small group of autistic children, also they only evaluated children with high-functioning which is consistent with the results of the present study [25, 22]. However, in this research, the appropriate effects of emotional facial education were investigated in autistic children with high and moderate functional levels. Hasanpour et al. conducted a study on 5 boys with high-functioning autism, as a single group with a “before and after approach” without considering the follow-up period. They found that although at the beginning of the study, children with autism in terms of facial emotional states performed poorly and scored low, after training in emotional facial recognition, they performed better in recognizing facial emotional states [25]. In addition, the results of this study are in line with the study by Conallen et al. that was conducted in one group with 10 autistic children with high functional levels. They reported that although in the pretest, these children weakly identified facial emotions, education during 10 sessions promoted the ability to recognize emotional states [24]. Silver et al. reported that Asperger’s children had difficulty distinguishing tired and thoughtful faces, but the education on the emotional states of the face had a significant positive impact on the ability of these children to identify facial emotions, which is consistent with the present study [26]. Also, Shiri et al. reported teaching facial expressions with a computer program improved the identification of facial emotions of joy, sadness, anger, and fear in autistic children with high functional levels [28]. Najafi et al. and Tanaka et al. also reported that teaching emotional facial expressions with a computer program significantly improved the identification of facial emotions in autistic children [23, 29], which is in line with this research. However, face-to-face relationship in these children was confined in these studies, which is inconsistent with the present study. This difference can probably be due to the participation of the coach and the mother in the training, the conversations, and the interactions during the training. Faja et al. also stated that facial education training has caused more attention from adults with autism to people’s faces, so basic perceptual skills training can be a promising educational method to promote the identification face emotions states in this group of patients [30]. On the other hand, Krysko and Rutherford showed that young children with autism have a poor performance in recognizing angry faces; this inability to recognize the angry moods of people around them sometimes causes their anger and harassment [31]. In the present study, it was also shown that children with autism have more difficulty in recognizing the emotional state of anger compared to other facial emotional states. However, the education caused the intervention group to perform better in identifying all emotional states of the face during the study.

5. Conclusion
Face emotions education could improve and promote identifying emotional states in children with autism, which ultimately increases the efficiency in the treatment of these children. In this regard, the caregivers and managers in health should use these findings to promote the relationship of children with autism with other people in the community and finally plan and adopt more comprehensive arrangements and plans.

Study limitations 
One limitation was the sudden onset of COVID-19, which prolonged sample collection. Examining the small number of children with autism was another limitation. So, researchers suggested for studying the exact effect of teaching facial expressions to children with autism further studies with more samples should be performed. Additionally, considering the effect of emotional face painting on the course and progress of treatment of autistic children, it is suggested that in various treatment interventions offered to children with autism, emotional face education should be developed along with treatment programs and its effect on adults should also be measured. Otherwise, this method should be done in adults as well.

Ethical Considerations
Compliance with ethical guidelines
This study received ethical approval from Hamadan University of Medical Sciences (No.: 1399.330), with the Iranian Registry of Clinical Trials (IRCT) (Code: 20190703044082N1). At the beginning of the study, the study objectives were explained to the participants and written consent was obtained from all mothers who participated in the present study.

Funding
Hamadan University of Medical Sciences financially supported this research.

Authors' contributions
Conceptualization and Supervision: Fateme Mohammadi, Fatemeh Cheragi, Fatemeh Mirzaei, Mahdieh Seyedi and Mohammad Rezaei; Investigation, Writing – original draft, and Writing – review & editing: Fateme Mohammadi, Fatemeh Cheragi, Fatemeh Mirzaei; Data collection: Fateme Mohammadi, Fatemeh Cheragi, Fatemeh Mirzaei, Mahdieh Seyedi and Mohammad Rezaei; Data analysis: Salman Khazaei. 

Conflict of interest
The authors declared no conflict of interest.

Acknowledgments
The authors would like to appreciate Hamadan University of Medical Sciences for financially supporting this research. The researchers would like to express their gratitude to the authorities at Hamadan School of Nursing and Midwifery, the parents of children with autism who participated in the study, and all the other individuals who cooperated with them.


References

1. Gurney JG, Fritz MS, Ness KK, Sievers P, Newschaffer CJ, Shapiro EG. Analysis of prevalence trends of autism spectrum disorder in Minnesota. Archives of Pediatrics & Adolescent Medicine. 2003; 157(7):622-7. [DOI:10.1001/archpedi.157.7.622] [PMID]
2. Benson PR. The impact of child symptom severity on depressed mood among parents of children with ASD: The mediating role of stress proliferation. Journal of Autism and Developmental Disorders. 2006; 36(5):685-95. [DOI:10.1007/s10803-006-0112-3] [PMID]
3. Sumiya M, Igarashi K, Miyahara M. Emotions surrounding friendships of adolescents with autism spectrum disorder in Japan: A qualitative interview study. Plos One. 2018; 13(2):e0191538. [DOI:10.1371/journal.pone.0191538] [PMID] [PMCID]
4. Jiujias M, Kelley E, Hall L. Restricted, repetitive behaviors in autism spectrum disorder and obsessive-compulsive disorder: A comparative review. Child Psychiatry & Human Development. 2017; 48(6):944-59. [DOI:10.1007/s10578-017-0717-0] [PMID]
5. Orme DM. A Qualitative examination of mothers' resolution or non-resolution of their childrens' disability of down syndrome or autism using a cognitive intervention. The Qualitative Report. 2005; 10(3):561-92. [DOI:10.46743/2160-3715/2005.1842]
6. Christensen DL, Braun KVN, Baio J, Bilder D, Charles J, Constantino JN, et al. Prevalence and characteristics of autism spectrum disorder among children aged 8 years-autism and developmental disabilities monitoring network, 11 sites, United States, 2012. Morbidity and Mortality Weekly Report. 2018; 65(13):1-23. [DOI:10.15585/mmwr.ss6513a1] [PMID] [PMCID]
7. Feldman MA, Werner SE. Collateral effects of behavioral parent training on families of children with developmental disabilities and behavior disorders. Behavioral Interventions. 2002; 17(2):75-83. [DOI:10.1002/bin.111]
8. Samadi SA, Mahmoodizadeh A, McConkey R. A national study of the prevalence of autism among five-year-old children in Iran. Autism. 2012; 16(1):5-14. [DOI:10.1177/1362361311407091] [PMID]
9. Ghorbani Moghanaki M. [The list of autism centers in the country was announced (Persian)] [Internet]. 2016. [Updated 2022 December 28]. Available from: [Link]
10. Nasseh H. [Along with autism, from diagnosis to treatment: For children who "want" but don't know how (Persian)]. Tehran: Danjeh; 2010. [Link]
11. Somerville M, Williams C. Sustainability education in early childhood: An updated review of research in the field. Contemporary Issues in Early Childhood. 2015; 16(2):102-17. [DOI:10.1177/1463949115585658]
12. Lacava PG, Golan O, Baron-Cohen S, Smith Myles B. Using assistive technology to teach emotion recognition to students with Asperger syndrome: A pilot study. Remedial and Special Education. 2007; 28(3):174-81. [DOI:10.1177/07419325070280030601]
13. Klin A, Jones W, Schultz R, Volkmar F, Cohen D. Visual fixation patterns during viewing of naturalistic social situations as predictors of social competence in individuals with autism. Archives of General Psychiatry. 2002; 59(9):809-16. [DOI:10.1001/archpsyc.59.9.809] [PMID]
14. Golan O, Baron-Cohen S, Ashwin E, Day K, McClintock S, Leggett V. Facilitating emotional understanding and face-processing in young children with autism spectrum conditions using animations of vehicles with faces. Poster presented at: British Psychological Scoiety Annual Conference. 2-4 April 2008. Dublin; Ireland. [Link]
15. Ashwin C, Baron-Cohen S, Wheelwright S, O’Riordan M, Bullmore ET. Differential activation of the amygdala and the ‘social brain’during fearful face-processing in Asperger syndrome. Neuropsychologia. 2007; 45(1):2-14. [DOI:10.1016/j.neuropsychologia.2006.04.014] [PMID]
16. Pelphrey KA, Sasson NJ, Reznick JS, Paul G, Goldman BD, Piven J. Visual scanning of faces in autism. Journal of Autism and Developmental Disorders. 2002; 32(4):249-61. [DOI:10.1023/A:1016374617369] [PMID]
17. Hill EL, Frith U. Understanding autism: Insights from mind and brain. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences. 2003; 358(1430):281-9. [DOI:10.1098/rstb.2002.1209] [PMID] [PMCID]
18. Howlin P. Interventions and outcome in Autism. International Perspectives on Child and Adolescent Mental Health. 2002; 2:69-99. [DOI:10.1016/S1874-5911(02)80004-5]
19. Fitzpatrick SE, Srivorakiat L, Wink LK, Pedapati EV, Erickson CA. Aggression in autism spectrum disorder: Presentation and treatment options. Neuropsychiatric Disease and Treatment. 2016; 12:1525-38. [DOI:10.2147/NDT.S84585] [PMID] [PMCID]
20. Farran EK, Branson A, King BJ. Visual search for basic emotional expressions in autism; impaired processing of anger, fear and sadness, but a typical happy face advantage. Research in Autism Spectrum Disorders. 2011; 5(1):455-62. [DOI:10.1016/j.rasd.2010.06.009]
21. Da Fonseca D, Santos A, Bastard-Rosset D, Rondan C, Poinso F, Deruelle C. Can children with autistic spectrum disorders extract emotions out of contextual cues? Research in Autism Spectrum Disorders. 2009; 3(1):50-6. [DOI:10.1016/j.rasd.2008.04.001]
22. Baron-Cohen S. The hyper-systemizing, assortative mating theory of autism. Progress in Neuro-Psychopharmacology and Biological Psychiatry. 2006; 30(5):865-72. [DOI:10.1016/j.pnpbp.2006.01.010] [PMID]
23. Tanaka JW, Wolf JM, Klaiman C, Koenig K, Cockburn J, Herlihy L, et al. Using computerized games to teach face recognition skills to children with autism spectrum disorder: The Let’s Face It! program. Journal of Child Psychology and Psychiatry. 2010; 51(8):944-52. [DOI:10.1111/j.1469-7610.2010.02258.x] [PMID]
24. Conallen K, Reed P. A teaching procedure to help children with autistic spectrum disorder to label emotions. Research in Autism Spectrum Disorders. 2016; 23:63-72. [DOI:10.1016/j.rasd.2015.11.006]
25. HasanPour M, Moradi V, Yaghoubnezhad S, Haghani S. [To investigate the effect of face emotion recognition training to children with high-functioning Autism on their mother-child relationship (Persian)]. Razi Journal of Medical Sciences. 2019; 26(6):54-63. [Link]
26. Silver M, Oakes P. Evaluation of a new computer intervention to teach people with autism or Asperger syndrome to recognize and predict emotions in others. Autism. 2001; 5(3):299-316. [DOI:10.1177/1362361301005003007] [PMID]
27. Boutet I, Faubert J. Recognition of faces and complex objects in younger and older adults. Memory & Cognition. 2006; 34(4):854-64. [DOI:10.3758/BF03193432] [PMID]
28. Shiri E, Nejati V, Poue Etemad H. [Investigation of the effectiveness of cognitive rehabilitation on improving the distinguishing of emotional states in children with high functioning autism disorder (Persian)]. Journal of Exceptional Children. 2013; 13(3):5-14. [Link]
29. Najafi M, Jafari Z, Mahaki B, Tootooni N. [Effect of let’s face it computer game on improving face recognition skills in patients with Autism spectrum disorders (Persian)]. Journal of Isfahan Medical School. 2016; 33(365):2279-87. [Link]
30. Faja S, Webb SJ, Jones E, Merkle K, Kamara D, Bavaro J, et al. The effects of face expertise training on the behavioral performance and brain activity of adults with high functioning autism spectrum disorders. Journal of Autism and Developmental Disorders. 2012; 42(2):278-93. [DOI:10.1007/s10803-011-1243-8] [PMID] [PMCID]
31. Krysko KM, Rutherford MD. A threat-detection advantage in those with autism spectrum disorders. Brain and Cognition. 2009; 69(3):472-80. [DOI:10.1016/j.bandc.2008.10.002] [PMID]