Epidemiology and diagnosis of attention deficit hyperactivity disorder in the Arab and Jewish populations in Israel

Aims: The aims of our study were to understand the factors shaping the gap in the literature concerning the Israeli Arab population, and to enhance the knowledge of Attention Defi cit Hyperactivity Disorder (ADHD) among this population, and provide information to health professionals. Methods: Retrospective data was collected from medical records in outpatient clinics between the years 2005-2017. Data included 474 Arab and 292 Jewish children aged 5 to 18 years. Results: Main reason for referral was inattention symptoms (44.4%) in Arabs, and academic problems (42.8%) in Jews. Arab preschoolers were mainly hyperactive, whereas adolescents complained about academic diffi culties. Arab girls reported inattention symptoms, whereas boys complained of aggressive behavior. ADHD combined subtype (ADHDC) was the most common subtype in both populations. ADHD-C was more prevalent in preschoolers, and ADHD Inattentive subtype (ADHD-I) was more prevalent between ages 11.1 to 15 years. We found an association between language delay and ADHD in both populations. Conclusion: ADHD characteristics among Israeli Arab and Jewish populations were mainly similar, and analogous with global results. Research Article Epidemiology and diagnosis of attention defi cit hyperactivity disorder in the Arab and Jewish populations in Israel Lutfi Jaber1,2*, Nasrin Hamed3, Ephraim S Grossman4 and Itai Berger5-7 1Department of Neurology and Child Development, Schneider Children’s Medical Center of Israel, Petah Tikva, Israel 2Sackler Faculty of Medicine, Tel Aviv University, Ramat Aviv, Israel 3Neuro-Pediatric Unit, Hadassah-Hebrew University Medical Center (Mount Scopus Campus), Jerusalem, Israel 4Department of Education, Ariel University, Ariel, Israel 5Pediatric Neurology at Assuta-Ashdod University Hospital, Ashdod, Israel 6Faculty of Health Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel 7The Paul Baerwald School of Social Work and Social Welfare, The Hebrew University of Jerusalem, Israel Received: 05 June, 2020 Accepted: 27 July, 2020 Published: 28 July, 2020 *Corresponding author: L Jaber MD, Professor, Department of Neurology and Child Development, Schneider Children’s Medical Center of Israel, Petah Tikva, Israel, Tel: +972-9-799-2655, 972-50-3377621; Fax: +972-9-799-5276; E-mail: ORCID: http://orcid.org/0000-0003-4599-3053


Introduction
Attention Defi cit Hyperactivity Disorder (ADHD) is the most common neurobehavioral disorder of childhood, and among the most prevalent chronic health conditions affecting schoolage children [1][2][3]. The prevalence rates of ADHD seem to have increased during the last decades [4,5]. Scientifi c research over the past 30 years has helped characterize biological and genetic components involved in ADHD [4]. Due to complexities regarding etiologic factors contributing to ADHD, researchers have studied the relationship of ADHD with various demographic factors, including race/ethnicity and Socioeconomic Status (SES) [6]. Rates of ADHD diagnosis, treatment, and access to care often appear to vary according to these factors. Not all studies have considered whether these factors confound one another [7]. Results have been inconsistent across studies investigating this issue. Basic information regarding how the prevalence of ADHD varies by race/ethnicity, sex, age and SES, remains poorly described [8].
In order to make a diagnosis of ADHD, the primary care clinician as well as other informants (parents, teachers, etc.) should determine (based on subjective judgement) that the Diagnostic and Statistical Manual of Mental Disorders (DSM) criteria have been met [9,10]. Thus, the behavioral characteristics may be interpreted differently by different observers and in diverse cultures [9][10][11]. Since the nature of this varies according to cultural as well as developmental and individual factors, we assume that diagnosis and treatment decisions will be more effective, and better accepted as researchers improve in identifying and managing ethnic and cultural parameters [12]. The predominance of American research into this disorder over the past 40 years has led to the impression that ADHD is primarily an American disorder and is much less prevalent elsewhere [13]. Similar characteristics and similar prevalence rates of ADHD have been found in different countries and cultures [2,14]. Dissimilarities may result from differential tolerance of inappropriate behavior across cultures, e.g. cross-cultural differences in authoritative parenting style could be relevant [15]. There are also signifi cant ethnic differences in knowledge and sources of information concerning ADHD and the use of out-of-school behavioral health services [16].
A review of epidemiology studies in Arab countries, using rating scales in a school setting, showed ADHD rates similar to those in other cultures [17]. Israel is a multiethnic country with a substantial minority of Arab and Druze citizens, and a large diverse immigrant population. One study showed a higher prevalence of ADHD in Jews compared to Arabs and Druze (3.6% vs.1.0%). This discrepancy could be due to genetic, environmental, cultural insensitivity, or under-diagnosis [18][19][20][21].
Socioeconomic factors interact with culturally based attitudes, and factors shape the pediatrician's willingness to issue prescriptions in response to both demands and public expectations [19]. Research suggests that culturally relevant factors, such as beliefs and values regarding child behavior, impact the way members of various ethnic and cultural groups view and respond to problematic behavior in children [22,23].
As all cultures tend to play a signifi cant role in shaping the individual's attitudes and behavior, particularly with regard to children's mental health, mental health professionals in general need to be knowledgeable about their patients by understanding their heterogenous cultural values, beliefs, and practices [24]. The aim of the current study was to understand the factors shaping the gap in the literature concerning the Israeli Arab population, as well as the paucity of information available regarding the risk and cultural factors, comorbidity, and the association with SES within the Arab community.

Summary
This is a descriptive observational study. As most published data are based on parent-teacher reports, our study used broader ADHD diagnostic determinations including clinicians' defi nitions to examine these relationships in a multisite sample. To enhance our understanding of ADHD in the Israeli Arab population, we identifi ed and retrospectively collected data on Arab and Jewish children aged 5 to 18 years, diagnosed with ADHD. These children had been referred to the ADHD Clalit Health Services Clinic between the years 2005-2017, and to the Hadassah-Hebrew University Medical Center between the years 2014 and 2016. Our aim was to identify the epidemiology, etiology and families' perceptions of their childrens' behavior.

Design
A two-stage study design was applied. In the fi rst phase, data was collected from the medical records of Arab patients. The diagnostic procedure relied on an interview with the patient and parents, a medical/neurological examination as described by the American Academy of Pediatrics clinical practice guidelines [25] and completion of ADHD symptom scales based on DSM-5 criteria [26]. The diagnostic process was performed by an indigenous Arabic speaking specialist in pediatric neurology in an outpatient clinic from January 2005 till December 2017. Data was collected from the Clalit Health Services which is the largest HMO in Israel.
In the second phase, data was collected from the medical records of Jewish children who were diagnosed in the same

Ethics statement
This study design was reviewed and approved by the

Statistical evaluation
Analysis of the data was performed using SPSS software to analyze quantitative data.
The analyses were performed on three levels:

Participants
Our cohort comprised 60.7% Arabs, and 39.1% Jews. ADHD was more prevalent among boys (Arabs 76.6%; Jews 70.9%) than among girls (Arabs 23.4%; Jews 29.1%). The Chi square test did not show a signifi cant difference in the incidence of ADHD by gender in either population.

Diagnosis
In both populations concern regarding the need for ADHD diagnosis was initiated more by the parents than the teachers.
Other informants in both populations were physicians, nurses, psychologists, speech therapists, and other family members (Table 1). When subtypes were defi ned based on DSM-5 criteria, the ADHD combined subtype (ADHD-C) was the most common subtype in the Arab population (50.1%) (  These results, presented in Table 4, suggested that when teachers were the original alerting source of information, they reported higher levels of ADHD symptoms in children.
Specialists also tended to report high levels of ADHD symptoms However, when parents were the original informants, they reported the lowest DSM-5 scores.
Furthermore, post-hoc comparisons confi rmed that the ratings of parents were signifi cantly lower than the ratings obtained from teachers.
For additional comprehension of the role played by the person who initiated the diagnosis, we performed an additional 2 x 3 (nationality x informant) ANOVA to test the differences in age of the child at fi rst referral for diagnosis. The results indicated a similar pattern for both nationalities. Interaction and main effect of nationality were not signifi cant, both with p values > 0.05. However, the main effect of informant was signifi cant (F(2,724) = 18.95, sig <0.001,  2 =0.05). The average age, combined for both nationalities, for fi rst referral for diagnosis was 8.61 (2.43) for cases initiated by teachers, 9.46 (3.30) for cases initiated by others groups, and highest 10.20 (3.24) for cases initiated by parents (Table 5).
In both populations there was a signifi cant relation between age groups and delay in developmental milestones. In the Arab preschool population (5 to 7 years) a Chi square test showed that this group was more prone to language delay (x 2 =9.35, df =3, sig 0.025) ( Table 6).
In our cohort most of the ADHD-diagnosed children exhibited diffi culties in combined learning objectives (reading, writing and calculating).
Among the ADHD-diagnosed children, the rate of cooccurrence with other psychopathological symptoms was higher in the Arab population despite no signifi cant relation according to Chi square in both populations. The most prevalent symptoms in the Arab population were: Conduct disorder (13%), oppositional defi ant disorder (ODD) (9%), seizures (2.6%), tics (1.3%), hearing diffi culties (2.6%). and enuresis (2%). In this same population there was a greater tendency for boys than girls with ADHD to suffer from sleep disorders (x 2 =3.37, df=1, sig=0.06).

Discussion
This study that compared parameters of pediatric ADHD in Israeli Arab and Jewish populations revealed that the    results of both populations were similar, and analogous with global results in most aspects. This study revealed that in the Arab sector the parents were the main informants, but low agreement was found between teachers and parents when teachers were the main informants. Such a divergence was not found in the Jewish population. Signifi cant differences were found between the two populations concerning chief complaint leading to a doctor's appointment in general, and age-related chief complaint. We found a relation between language delay and ADHD in both populations.
The differences in symptoms in relation to age and gender in this study are similar to other studies. As was concluded previously, the fi rst steps towards seeking help for a child with ADHD lies in identifying core symptoms and assessing impairment level (1). In our study, in the Arab and Jewish populations, parents and not teachers reported a higher prevalence of ADHD symptoms. This fi nding is appropriate for the Arab culture, where parents (especially the mother) are the primary caretakers [27].
We also found that when teachers were the original alerting source of information, they reported higher levels of ADHD symptoms in children than did the parents. This implies that parent-teacher agreement on ADHD rates was low when the parents were not the informants. Low parentteacher agreement on ADHD rates was also shown in other cultures [28,29]. Sollie, et al. [28] found that according to the hyperactivity-impulsivity subscale on the ADHD rating scale-IV, teachers rated the child's problems to be less serious than did both parents, which contradicts the results of the study conducted in an Arab population [30][31][32]. Our fi ndings indicated that more Arab children may suffer from unrecognized behavioral problems, and moreover, could explain the higher prevalence of Jewish ethnicity reported by Farbstein, et al. [18].
Differences were found both on DSM-5 scores and age between cases in which parents vs teachers initiated the quest for ADHD diagnosis. Teachers referred younger children and reported higher scores than parents. It may be asserted that the more severe cases were identifi ed at an earlier stage. Teachers recognized ADHD symptoms in those children and requested referral for treatment even before parents became aware of any warning signs. On the other end of the spectrum were the children with less severe ADHD who remained undiagnosed till a later stage when the parents, for any reason, were ready to seek help.
Regarding the persistence of ADHD symptoms throughout development, there is a continuance of inattention symptoms, whereas levels of hyperactivity decrease with age [33][34][35].
Poor concentration and high levels of activity are frequent characteristics of normal preschool children. At school age the child starts developing maturity that facilitates learning and concentration. According to Larsson, et al. [33], variations in symptoms between childhood and early adolescence are not only due to new genetic effects but also due to new non-shared environmental effects that gain importance during adolescence. Our study replicated these fi ndings in Arab preschoolers. Hyperactivity symptoms were more consistently reported by different informants at school age  [27] found that ADHD was associated with low grades, reading problems, and poor performance in mathematics standardized test scores, and with an increased likelihood of repeating a school year. Thorell [36], reported that only symptoms of inattention were correlated with academic skills. We speculated that the reasons for the emergence of academic problems at an earlier age in the Jewish population were connected to differences in the awareness of ADHD, a point which is beyond the scope of this paper.
As was previously published ADHD symptoms in our study were gender related. Arab girls complained more about inattention whereas boys reported aggression. This fi nding is consistent with other studies which showed that, according to parents and teachers, boys were more likely to be hyperactive, whereas girls tended to be inattentive [32]. Similarly, other researchers confi rmed that the inattentive subtype is more prevalent in girls [37][38][39].
Concerning subtypes, we found that the rates of the inattentive, hyperactive-impulsive, and the combined subtypes were 34.4%, 0.2% and 50.0%, respectively, in both populations, with the combined subtype being the most prevalent.
Surprisingly, different fi ndings were reported internationally, with the predominance of the inattentive subtype [40,41].
Regarding subtypes and age groups, in preschoolers, as found in other studies, the hyperactive-impulsive subtype is the most prevalent [29,43]. In the school age group, the inattentive subtype outweighed the other subtypes, which correlates with other studies conducted in Israel and worldwide [44].
However some results are different to those previously together with the long-lasting Palestinian-Israeli confl ict make this country unique in comparison with other cultures [42]. Therefore, further studies might be needed in order to investigate the reason for these differences in both Israeli and global populations.
We found that delayed language development was an early sign of ADHD among the Jewish population. Whereas this result correlates with that of another study conducted in Israel [45], in our Arab population sample, as well as in other studies, there was no signifi cant relation between delayed language development and ADHD [29]. More studies are warranted in examining the long-term outcome of language delay and ADHD symptoms, especially attention defi cit and its effect on language, short term memory and processing speed.
Our study has several limitations: This study was based on data from a single institution for each ethnicity. The majority of cases were boys, which could cause a bias, as there is under diagnosis amongst girls who tend to be less disruptive. Despite the existence of differences in the prevalence of ADHD among socioeconomic levels internationally, these differences did not reach a signifi cant level due to the lack of heterogeneity in the SES index of the Arab localities, which were found to be in the lower SES indices.

Conclusion
Our study revealed that in most aspects, the results of the Israeli Arab and Jewish populations were similar, and analogous with global results. However, there are some differences between our study and international studies, which warrants further investigation. Ethnic and cultural differences may explain some of the increase in ADHD prevalence worldwide. In Israel, as in other countries, efforts are being made to enhance physicians' sensitivity to the diagnosis of ADHD and ethnic/cultural differences. Increased public awareness, improved access to health services, and improved referral from primary care and communities to specialty health services may increase the likelihood of ADHD being identifi ed on screening and diagnosis [19,46]. The contributions of these parameters and the understanding of the complex relationships between ethnic/cultural variables and ADHD identifi cation and treatment warrant further investigation and may aid clinicians in providing more specifi c and appropriate care [7,46].

Author contributions
LJ and NH contributed equally to this work as the principal investigators. LJ, NH and IB conceptualized, designed the study and drafted the initial manuscript. NH and EG completed the statistical analyses. NH and LJ collected the data. EG assisted with the statistical analyses. LJ, NH, and IB critically reviewed and revised the manuscript. All authors were involved in writing the paper and had fi nal approval of the submitted and published versions.