Study design
Our study was a cross-sectional study. It was carried out in the period between October 2019 and October 2020.
Participants
Children and adolescents with type 1 diabetes aged 6 to 16 years old were randomly recruited from the Pediatric Diabetes Clinic of Ain Shams University Children’s’ Hospital. These children and adolescents were randomly selected using simple random sampling from the clinic data base. Type 1 diabetes was diagnosed if the patient was not obese, had no signs of insulin resistance, no family history suggestive of MODY (monogenic or maturity onset diabetes of the young), had low C-peptide, and showed insulin dependency on the doses required for a T1DM patient. Autoantibody testing is performed at our center if any of the aforementioned criteria is not fulfilled. Patients who did not have any of the exclusion criteria were first extracted from the clinic database. Next, from those patients, a sample was randomly selected for inclusion in the study using a simple random technique by means of a random number generator software. Exclusion criteria included having any neurologic disease, developmental disorder, learning disability, hearing or visual impairment, sleep disorder, specific emotional or behavioral disorders (e.g., anxiety, depressive, oppositional defiant, and conduct disorders), thyroid disease or any other chronic illness (other than diabetes), or having a positive family history of ADHD or other psychiatric disorder. Moreover, psychiatric evaluation was not done following recent recovery from diabetic ketoacidosis.
Age and sex-matched healthy controls were recruited from the outpatient clinic of the Ain Shams University Children’s’ Hospital. They were either coming for their scheduled vaccinations or to follow-up their growth.
A required sample size of 70 cases with type 1 diabetes and 70 controls was calculated using the Epitools program setting to detect an alpha error at 5% and power at 80%.
Data collected and study tools
Data on history of diabetes mellitus duration, current age and age at onset of diabetes, dosage of insulin, method of insulin delivery, and HbA1c average over the 6 month-period prior to inclusion in the study were collected. Diabetes control was classified as follows: good control if HbA1c < 7.5%, borderline if HbA1c is between 7.5 and < 9%, and poor control if at or above 9%. This is based on the American Diabetes Association guidance and the International Society of Pediatric and Adolescent Diabetes (ISPAD) guideline [7] advising such higher HbA1c goal if there is lack of access to advanced insulin delivery technology and continuous glucose monitoring (CGM) for the child with diabetes [7].
Psychometric assessment for ADHD
The following assessments were used in evaluating possible ADHD diagnosis among children and adolescents with type 1 diabetes and controls:
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A.
Pediatric Symptom Checklist (PSC)—the Arabic validated version [8].
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B.
Diagnostic and Statistical Manual of Mental Disorders—the fifth edition (DSM-5) criteria. DSM-5 criteria are the standard criteria used based on the best available evidence for ADHD diagnosis [9, 10]. The Arabic validated version was used [11].
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C.
Conners comprehensive behavior rating scale—revised for parents/caregivers: the Arabic validated version [12].
A. Pediatric Symptom Checklist (PSC)—parent version
This is a brief, 35-item, questionnaire designed to screen for cognitive/attention, emotional, and behavioral problems in children and adolescents and is meant to provide an assessment of psychosocial functioning. Although psychosocial problems are relatively common in pediatrics, they may not be noticed by teachers, pediatricians, and even parents. Therefore, the American Academy of Pediatrics recommends psychosocial screening as a part of the annual physical assessment for all children and adolescents. Items are scored on a scale of 0, 1, and 2 as “never,” “sometimes,” and “often,” respectively. For children aged 6 to 15, scores at or above a cutoff of 28 indicate the presence of impaired psychosocial functioning compared to most other children of the same age and the need for further professional assessment [8]. The checklist takes around 5 min to fill out. The Arabic version was used [8]. Translations were created for the California Department of Health Services, where the original PSC was developed and are available on their website [8].
B. DSM-5 criteria for ADHD [9, 10]
Children or adolescents are classified as either having primarily inattentive type of ADHD or primarily hyperactive-impulsive type or a combined diagnosis of both if criteria of both are present.
Primarily inattention type is diagnosed in the age group of 6–16 years of age if six or more symptoms of inattention have been present for at least 6 months. These include:
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Fails to give close attention to details or makes careless mistakes in schoolwork, at work, or with other activities
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Has trouble holding attention on tasks or play activities
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Does not seem to listen when spoken to directly
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Does not follow through on instructions and fails to finish schoolwork, chores, or duties in the workplace (e.g., loses focus, side-tracked)
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Has trouble organizing tasks and activities
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Avoids, dislikes, or is reluctant to do tasks that require mental effort over a long period of time (such as schoolwork or homework)
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Loses things necessary for tasks and activities (e.g. school materials, pencils, books, tools, wallets, keys, paperwork, eyeglasses, mobile telephones)
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Is easily distracted
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Is forgetful in daily activities
Predominantly hyperactive/impulsive type is diagnosed in the age group of 6–16 years if six or more symptoms of hyperactivity-impulsivity have been present for at least 6 months.
Hyperactive symptoms include:
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Often fidgets with or taps hands or feet, or squirms in seat
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Often leaves seat in situations when remaining seated is expected
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Often runs about or climbs in situations where it is not appropriate (adolescents or adults may be limited to feeling restless)
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Often unable to play or take part in leisure activities quietly
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Is often “on the go” acting as if “driven by a motor”
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Often talks excessively
Impulsive symptoms include:
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Often blurts out an answer before a question has been completed
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Often has trouble waiting their turn
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Often interrupts or intrudes on others (e.g., butts into conversations or games or activities)
Combined type is diagnosed if at least 6 symptoms of both inattention and hyperactivity/impulsivity are present for at least 6 months.
Whatever the type, symptoms must be present and impair proper functioning in at least two settings (school, home, sport, etc.) and must start before reaching the age of 12 years. Also, the child must not have any other comorbid disorder that may cause such symptoms (mental, developmental, psychiatric, or sleep disorder).
The validated form of the Arabic version of DSM-5 [11] was used and was completed by the parent (mostly the mother).
C. Conners rating scale-revised, long version—parent scale
Conners Parent Rating Scale-revised (CPRS-R), long version, is an assessment tool used to detect symptoms of ADHD and to classify its' subtypes based on the parent’s observations about the youth’s behavior [12]. It is an 80-question tool, and parent responses are scored based on the frequency of occurrence of the symptom from 0 (not true or rarely true) to 3 (very true or very often true). It is completed by most parents within 20 min [13]. A standardized T score is calculated where the average scores range usually falls between 40 and 59 (within one standard deviation of mean). Scores from 60 to 64 are considered borderline or “high average” (within 1–1.5 standard deviations above mean) and require careful clinical judgment. Scores in the range of 65–69 are in the “elevated” range and usually indicate more concern than is typically reported. T scores at or above 70 (> 2 standard deviations above the mean, “very elevated” range) are very likely indicative of a significant area of concern [14].
The scale assesses a variety of behavioral problems in children and adolescents, including oppositional, cognitive problems/inattention, hyperactivity, anxious-shy, perfectionism, social problems, and psychosomatic behavioral problems. Several subscale indices are calculated from the scale, including an ADHD Index, three DSM-IV symptoms’ indices, and Conners global indices. The ADHD index is useful in identifying children and adolescents who may meet DSM-5 criteria for ADHD. There is strong evidence for ADHD when the ADHD index, the DSM Symptoms’ Indices, the Hyperactivity Subscale, and the Cognitive Problems/Inattention Subscales are all elevated [13].
It is important to note that combining information gathered from each psychometric measure together with interviews, observations, and review of available records is needed and gives the assessor a more comprehensive view of the youth than might be obtained from any one source, so that correct decisions can be made.
Statistical analysis
The collected data were revised, coded, and introduced using IBM SPSS Statistics version 17. Continuous variables were represented by the mean and standard deviation, while categorical variables were represented by percentages. Non-normally distributed variables were represented as median and interquartile ranges. Comparisons between the groups were made using an unpaired t-test, analysis of variance, or Wilcoxon signed rank tests for continuous variables and chi-squared test for categorical variables; p value of less than 0.05 was considered statistically significant.
