ABSTRACT
Background:
Global developmental delay (GDD) is a common pediatric condition with multiple etiologies. An electroencephalogram (EEG) is commonly used, when there is a clinical suspicion of seizures in GDD, which provide treatment options and a prognosis. Aims: To study the prevalence of EEGs findings in pediatric patients presenting with GDD and to examine the use of abnormal EEGs assessment in children with GDD. Design: A retrospective cross-sectional study. Settings: Pediatric neurology clinic at king Fahad specialist hospital in Dammam (KFSHD), Saudi Arabia.
Methods and Materials:
The data consist of brain EEGs of 110 patients who were referred by the pediatric neurology department from February 2016 to April 2018. The data entered and analyzed by using Statistical package for the social sciences (SPSS).
Results:
The sample is a total of 110 pediatric patients, 59 males and 51 females, who were diagnosed with developmental delay. The mean age of children with abnormal EEG findings was 22.5 months ± 60.5, with a range of three months to 12 years. The oldest age group was five to 12 years, with a P value of 0.001. Seventy-nine percent of the participants had abnormal EEGs; 20.90% had normal EEGs. In 53 patients (61%), the EEG plays an important role in the clinical assessment that was confirmed by further investigation; the P value for this finding was 0.001.
Conclusion:
An EEG played important role to classify seizures in children with GDD. Brain EEGs can demonstrate the association of brain anomalies with the etiologies of GDD and increase the rate of positive outcomes for children with GDD.
Keywords: Developmental delay, electroencephalography, language and speech disorders
Introduction
The incidence of global developmental delay (GDD) in children under five years is estimated to be around one to three percent.[1] Few studies have been done on GDD in Saudi Arabia; 2019 retrospective study in Saudi Arabia aimed to assess the patterns of GDD in 134 pediatric patients.[2]
GDD is continuous process that begins at conception and continues until maturity. Several factors, including genetic, environmental, and nutritional factors, as well as, chronic diseases, can adversely affect development and delay developmental milestones. These milestones are categorized into four domains: Gross motor skills, fine motor skills, social skills, and linguistic skills.[3] An individual’s degree of developmental delay is further classified as mild (functional age <33% lower than chronological age), moderate (functional age 34%-66% of chronological age) and severe (functional age <66% of chronological age).[4] In summary, GDD is neither a disease nor a diagnosis; it is a symptom or clinical presentation.[3,4,5,6,7,8]
GDD is a common pediatric condition with highly heterogeneous etiologies; however, the etiology of GDD can be identified in 40% to 80% of cases.[9] Developmental delay may become evident during infancy or early childhood, but it becomes more apparent later and is usually diagnosed in the early school years.[10] The early proper diagnosis can help the better treatment option and provide a prognosis and condition-specific family support (including family planning choices).[11] A diagnosis may also provide an explanation, helping parents achieve closure or acceptance and it eliminates the need for clinicians to proceed to potentially more expensive and invasive tests.[12,13,14]
A brain electroencephalogram (EEG) plays an important role in the clinical neurophysiological assessment of a child with GDD. According to previous studies, about 60% of children with GDD have abnormal EEGs.[15,16,17,18] In some cases, clinical findings may provide a diagnosis, but for most cases, an EEG is necessary to provide a picture of the abnormality.
Primary care physicians play a major role in early detection of developmental delays, through developmental monitoring and screening. Therefore, it is necessary that they have the experience and skills to detect GDD and provide a proper guidance and counseling to the parents.[19,20]
The present study aimed to characterize the neurophysiological assessment of EEGs and the prevalence of normal and abnormal EEG in pediatric patients presenting with GDD.
Methodology
Methods and materials
A retrospective review of the charts of 110 children diagnosed with GDD in the pediatric neurology and development assessment clinic at King Fahd Specialist Hospital Dammam (KFSHD) between Feb 2016 and April 2018 was conducted. Permission was obtained from the KFSHD local ethics committee. The participants were identified through a review of the charts of all patients assessed in the Developmental Progress Clinic during the study time period. Referrals to the clinic come mainly from pediatricians, family physicians, and pediatric neurology departments in the eastern province region.
In previous study, we have described the procedure of enrolling the subject “all children referred to the clinic undergo a formal multidisciplinary developmental assessment (complete history and a developmental pediatrics examination)”.[2] A detailed neurologic examination was performed by a pediatric neurologist, and the results of any previous neuroimaging were documented in a predesigned pro forma document.
In all included patients, a standard EEG was performed for a minimum of 40 minutes to capture both wakefulness and sleep in stages. Bipolar and referential montages were used, as recommended in the 10:20 international system of recording and the ACNS (American Clinical Neurophysiology Society) guidelines. The EEG recordings were reviewed by a trained pediatric neurologist. For each EEG, age-appropriate EEG characteristics; benign variants; and abnormalities, including interictal epileptiform discharges and ictal discharges, if any, were identified. Focal or diffused hyperactive epileptic activity, along with its localization and temporal characteristics, were specifically highlighted. According to the International Federation of Societies for Electroencephalography and Clinical Neurophysiology (IFSECN), epileptiform waves or activity are “distinctive waves or complexes, distinguished from background activity, and resembling those recorded in a proportion of human subjects suffering from epileptic disorders”.[18] A detailed history was obtained for all patients, and the patients were diagnosed for developmental delay. Both sexes were included in the study.
Inclusion criteria
Children of 3 month-12 years of age presenting with development delay.
Exclusion criteria
Patients with autism and non-cooperative for development assessment.
Absence of the complete data set of the patient as designed in the clinical evaluation sheet.
Statistical analysis
The SPSS software version 22.0 (SPSS Inc., Chicago) were used for analyzing the data. A P value of 0.05 or less was considered to be statistically significant.
Results
A total of 110 pediatric patients, 59 male and 51 female (male: Female ratio, 1.15:1) who were diagnosed with developmental delay were included in this study. The study aimed to assess the usefulness of an EEG as a diagnostic tool for children with GDD.
Twenty-three of the participants (20.9%) presented with normal EEGs; of these, 15 (65.3%) were male and eight (34.7%) were female. The remaining 87 participants (79.1%) presented with abnormal EEGs; of these, 44 (50.6%) were male and 43 (49.4%) were female. The male-to-female ratio of those with abnormal EEGs was 1.02:1, similar to the overall ratio. No statistically significant gender difference was found between the normal and abnormal EEG patients (p = 0.21) [Table 1].
Table 1.
Age and sex distribution of study population with normal and abnormal EEG
| Parameter | Abnormal EEG findings (n=87) | Normal EEG findings (n=23) | P | ||
|---|---|---|---|---|---|
|
|
|
||||
| Frequency | Frequency | Percentage | |||
| Age | |||||
| 3 months-1 years | 5 | 5.7 | 0 | 0 | P=0.01 |
| 1-2 years | 12 | 13.7 | 1 | 4.3 | |
| 2-5 years | 21 | 24.1 | 4 | 17.3 | |
| 5-8 years | 25 | 28.7 | 12 | 52.1 | |
| 8-12 years | 24 | 27.5 | 6 | 26 | |
| Sex | |||||
| Males (n=59) | 44 | 50.6 | 15 | 65.3 | P=0.21 |
| Females (n=51) | 43 | 49.4 | 8 | 34.7 | |
The mean age of children with abnormal EEG findings was 22.5 months (standard deviation [SD]: 60.5; age range: Three months to 12 years). The oldest age groups were five to eight years and eight to 12 years, representing 28.7% and 27.5% of the patients, respectively. Levene’s test indicated a statistically significant difference in the ages of patients with normal and abnormal EEGs (p = 0.001).
Of the 87 children diagnosed with GDD and abnormal EEGs, an EEG provided a direct diagnosis in 53 patients (61%). The remaining 34 patients (39%) presented with non-specific abnormalities in the EEG (p = 0.001) [Table 2].
Table 2.
Types of EEG findings in abnormal EEG group
| Parameter | Abnormal EEG findings (n=87) | P | |
|---|---|---|---|
|
| |||
| Frequency | Percentage | ||
| Specific EEG abnormality | 53 | 61 | P=0.001 |
| Non-Specific EEG abnormality | 34 | 39 | |
Discussion
Since this study was conducted in a hospital, it may not reflect the actual situation as well as a community-based study. The study aimed to examine the prevalence of normal and abnormal EEGs help in neurophysiology assessment in children with GDD and to investigate how abnormal EEGs help diagnose children with GDD. The aim was to identify specific abnormalities that can provide an accurate diagnosis and further help define proper treatment options that support the best overall outcomes.
A sample of 110 pediatric patients three months to 12 years were evaluated for developmental delay. Of this sample, 79.1% presented with abnormal EEGs. A similar finding was reported in a cohort study conducted in Nigeria in 2008.[16] In that study, of 111 patients diagnosed with developmental disorders, 80.2% presented with EEG abnormalities. That study found no statistically significant association between abnormal EEGs and diagnoses of developmental abnormalities, except for mixed specific developmental disorder (observed in 55% of the sample) and specific developmental disorders of speech and language (present in 34.2%) (p = 0.01). The most common complication was seizures, which occurred in 20% of the patients. The high proportion of EEG abnormalities in these participants may be explained by subtle brain damage, the likely cause of developmental disorders as well as the associated complications such as seizures and mixed specific developmental disorder.[16]
In a 2012 study in Oman, 59.1% of GDD patients presented with EEG abnormalities.[6] In a 2019 study in Saudi Arabia, 45% of patients diagnosed with GDD presented with EEG abnormalities.[2] In a 2017 study in the United Kingdom, abnormal EEGs were observed in 47.9% of children with speech and language impairments.[1] Because similar EEG abnormalities have been observed in children with speech and language impairments, an EEG can estimate the prognosis for these patients.[21] In another study, conducted in Japan in 2014, almost half of children diagnosed with ADHD (48.3%) presented with EEG abnormalities.[22] The wide range in these previous findings could be due to differences in the population, selection criteria, and extent of these studies.
The children with abnormal EEGs in our study were aged between three months and 12 years, with a mean age of 22.5 months. The age at which GDD presented in our sample was similar to that observed in previous studies.[23,24,25,26] Our male-to-female ratio of 1.15:1 was also similar to that of one other study[6]; many other previous studies had higher male to female ratio.[7,16,17,22] No statistically significant gender-related differences appeared in the abnormal EEG group (p > 0.05), as in a previous similar study (p-value = 0.84).[1]
In our study, an EEG provided a direct diagnosis in 53 children with GDD and abnormal EEGs (61%); these diagnoses were confirmed by further investigation. The remaining 34 patients (39%) had non-specific EEG abnormalities. An EEG plays an essential role in assessing children with developmental delays; the etiological yield and the specificity of the diagnosis can be increased if other associated clinical and neurological signs and symptoms are included in the criteria for diagnosis.[5,11] Another study reported that, of patients with abnormal EEGs (47.9%, n = 45/94), 64.5% had abnormal background activity. Epileptiform EEG changes were observed in all patients with a history of seizures (73.6%, n = 14/19) and in almost half of those without a history of seizures (41.3%, n = 31/75) (p-value = 0.01).[1] This high epileptiform in the EEG findings demonstrates that seizures (epilepsy) can be associated with developmental delay, provide a direct diagnosis of developmental delay, or appear as an additional manifestation.[25] An EEG plays an important role in the comprehensive evaluation of children with developmental delays.[14,15,16,17,18,27,28,29] However, in contrast to this, one study in Oman found no significant association between EEG abnormalities and detection of etiology.[6] As mentioned above, these contradictory findings could be due to differences in the population, criteria, and extent of various studies.
Conclusion
The present study has some limitations, including its retrospective design and the relatively small number of subjects, all of whom were evaluated at a single center. A prospective study using a larger sample is needed to further explore the role of EEGs in diagnosing GDD.
GDD is a common pediatric condition with multiple etiologies; the cause can be identified in up to 80% of cases. An EEG plays an important role in the comprehensive evaluation of children with developmental delays and contributes to diagnosis as many specific etiologic and pathophysiologic conditions that lead to developmental delays can be easily detected in an EEG. Brain EEGs help clinicians provide proper diagnoses, leading to appropriate, early treatment of developmental disorders and the best overall outcomes.
Key points
EEGs can demonstrate the association of brain anomalies with the etiologies of GDD
The EEG can provide assesment, which is key to proper treatment
The children with abnormal EEGs in our study were aged between three months and 12 years which was similar to that observed in previous studies.
Conflicts of interest
There are no conflicts of interest.
Acknowledgments
The authors would like to thank Brent L Hedgcock, our lead EEG technologist for his technical help.
Funding Statement
Nil.
References
- 1.Mithyantha R, Kneen R, McCann E, Gladstone M. Current evidence-based recommendations on investigating children with global developmental delay. Arch Dis Child. 2017;102:1071–6. doi: 10.1136/archdischild-2016-311271. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.Habibullah H, Albradie R, Bashir S. Identifying pattern in global developmental delay children: A retrospective study at King Fahad specialist hospital, Dammam (Saudi Arabia) Pediatr Rep. 2019;11:8251. doi: 10.4081/pr.2019.8251. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 3.Shevell M, Ashwal S, Donley D, Flint J, Gingold M, Hirtz D, et al. Practice parameter: Evaluation of the child with global developmental delay: Report of the quality standards subcommittee of the American academy of neurology and the practice committee of the child neurology society. Neurology. 2003;60:367–80. doi: 10.1212/01.wnl.0000031431.81555.16. [DOI] [PubMed] [Google Scholar]
- 4.McDonald LA, Rennie AC. Investigating developmental delay/impairment. J Paediatr Child Health. 2011;21:443–47. [Google Scholar]
- 5.Petersen MC, Kube DA, Palmer FB. Classification of developmental delays. Semin Pediatr Neurol. 1998;5:2–14. doi: 10.1016/s1071-9091(98)80012-0. [DOI] [PubMed] [Google Scholar]
- 6.Koul R, Al-Yahmedy M, Al-Futaisi A. Evaluation children with global developmental delay: A prospective study at sultan Qaboos university hospital, Oman. Oman Med J. 2012;27:310. doi: 10.5001/omj.2012.76. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Battaglia A, Bianchini E, Carey JC. Diagnostic yield of the comprehensive assessment of developmental delay/mental retardation in an institute of child neuropsychiatry. Am J Med Genet. 1999;82:60–66. [PubMed] [Google Scholar]
- 8.Williams HJ. Imaging the child with developmental delay. Br J Radiol. 2004;16:174–85. [Google Scholar]
- 9.Bélanger SA, Caron J. Evaluation of the child with global developmental delay and intellectual disability. J Paediatr Child Health. 2018;23:403–10. doi: 10.1093/pch/pxy093. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Curry CJ, Stevenson RE, Aughton D, Byrne J, Carey JC, Cassidy S, et al. Evaluation of mental retardation: Recommendations of a consensus conference. Am J Med Genet. 1997;72:468–77. doi: 10.1002/(sici)1096-8628(19971112)72:4<468::aid-ajmg18>3.0.co;2-p. [DOI] [PubMed] [Google Scholar]
- 11.Ballaban-Gil K, Tuchman R. Epilepsy and epileptiform EEG: Association with autism and language disorders. Ment Retard Dev Disabil Res Rev. 2000;6:300–8. doi: 10.1002/1098-2779(2000)6:4<300::AID-MRDD9>3.0.CO;2-R. [DOI] [PubMed] [Google Scholar]
- 12.Echenne B, Cheminal R, Rivier F, Negre C, Touchon J, Billiard M. Epileptic electroencephalographic abnormalities and developmental dysphasias: A study of 32 patients. Brain Dev. 1992;14:216–25. doi: 10.1016/s0387-7604(12)80233-6. [DOI] [PubMed] [Google Scholar]
- 13.Panayiotopoulos CP, Michael M, Sanders S, Valeta T, Koutroumanidis M. Benign childhood focal epilepsies: Assessment of established and newly recognized syndromes. Brain. 2008;131:2264–86. doi: 10.1093/brain/awn162. [DOI] [PubMed] [Google Scholar]
- 14.Mehta B, Chawla VK, Parakh M, Bhandari B, Gurjar AS. ABER assessment in pre-school children with developmental speech and language impairment. J Clin Diagn Res. 2015;9:CC01–3. doi: 10.7860/JCDR/2015/13723.5873. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Lévy-Rueff M, Bourgeois M, Assous A, Beauquier-Maccota B, Boucheron E, Clouard C, et al. Abnormal electroencephalography results and specific language impairment: Towards a theoretical neurodevelopmental model? Encephale. 2012;38:318–28. doi: 10.1016/j.encep.2011.12.008. [DOI] [PubMed] [Google Scholar]
- 16.Aina OF, Ogun OC, Ladapo HT, Lesi FE, Famuyiwa OO. Clinical neuropsychiatric correlates and EEG findings among children with developmental disorders in Lagos, Nigeria. Afr J Psychiatry (Johannesbg) 2008;11:123–7. doi: 10.4314/ajpsy.v11i2.30264. [DOI] [PubMed] [Google Scholar]
- 17.Tuchman RF, Rapin I. Regression in pervasive developmental disorders: Seizures and epileptiform electroencephalogram correlates. Paediatrics. 1997;99:560–6. doi: 10.1542/peds.99.4.560. [DOI] [PubMed] [Google Scholar]
- 18.IFSECN International federation of societies for electroencephalography and clinical neurophysiology. A glossary of terms most commonly used by clinical Electroencephalographers. Electroencephalogr Clin Neurophysiol. 1974;37:538–48. doi: 10.1016/0013-4694(74)90099-6. [DOI] [PubMed] [Google Scholar]
- 19.Choo YY, Agarwal P, How CH, Yeleswarapu SP. Developmental delay: Identification and management at primary care level. Singapore Med J. 2019;60:119–23. doi: 10.11622/smedj.2019025. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Khan I, Leventhal BL. In: StatPearls [Internet] Treasure Island (FL): StatPearls Publishing; 2020. Developmental delay. [Google Scholar]
- 21.Shewmon DA, Erwin RJ. Focal spike-induced cerebral dysfunction is related to the after-coming slow wave. Ann Neurol. 1988;23:131–7. doi: 10.1002/ana.410230205. [DOI] [PubMed] [Google Scholar]
- 22.Kanazawa O. Reappraisal of abnormal EEG findings in children with ADHD: On the relationship between ADHD and epileptiform discharges. Epilepsy Behav. 2014;41:251–6. doi: 10.1016/j.yebeh.2014.09.078. [DOI] [PubMed] [Google Scholar]
- 23.Picard A, Cheliout Heraut F, Bouskraoui M, Lemoine M, Lacert P, Delattre J. Sleep EEG and developmental dysphasia. Dev Med Child Neurol. 1998;40:595–9. doi: 10.1111/j.1469-8749.1998.tb15424.x. [DOI] [PubMed] [Google Scholar]
- 24.Battaglia A, Carey JC. Diagnostic evaluation of developmental delay/mental retardation: An overview. Am J Med Genet C Semin Med Genet. 2003;117:3–14. doi: 10.1002/ajmg.c.10015. [DOI] [PubMed] [Google Scholar]
- 25.Pandey A, Phadke SR, Gupta N, Phadke RV. Neuroimaging in mental retardation. Indian J Pediatr. 2004;71:203–9. doi: 10.1007/BF02724269. [DOI] [PubMed] [Google Scholar]
- 26.Moes P, Schilmoeller K, Schilmoeller G. Physical, motor, sensory and developmental features associated with agenesis of the corpus callosum. Child Care Health Dev. 2009;35:656–72. doi: 10.1111/j.1365-2214.2009.00942.x. [DOI] [PubMed] [Google Scholar]
- 27.Bednarek N, Motte J. Developmental delay and epilepsy. Epileptic Disord. 2006;8:17–21. [Google Scholar]
- 28.Binnie CD, de Silva M, Hurst A. Rolandic spikes and cognitive function. Epilepsy Res Suppl. 1992;6:71–73. [PubMed] [Google Scholar]
- 29.Deonna T, Zesiger P, Davidoff V, Maeder M, Mayor C, Roulet E. Benign partial epilepsy of childhood: A longitudinal neuropsychological and EEG study of cognitive function. Dev Med Child Neurol. 2000;42:595–603. doi: 10.1017/s0012162200001122. [DOI] [PubMed] [Google Scholar]
