Assessment of neurological development in children with hydrocephalus
Keywords:
progressive hydrocephalus, electrical status of slow-wave sleep, SWI-index (spike-wave index), MMSE (The Mini-Mental State Examination), GMFCS (Gross Motor Function Classification System), electroencephalography, magnetic resonance imaging, cerebrospinal fluid shunt system.Abstract
Today, the world is actively developing a multidisciplinary approach to children with hydrocephalus by assessing the electrophysiological, radiological and clinical indicators of cognitive and motor development of children. Progressive hydrocephalus is one of the urgent conditions that can be life threatening, especially in early childhood [1-3]. Often this process is accompanied by epileptic seizures. The prevalence of the latter in children with hydrocephalus is from 20 to 50% [3]. It was found that the presence of epileptic seizures leads to a worsening of the prognosis of cognitive and motor development in children [2-10]. According to current data in the world literature, the indicators of electroencephalogram data are important for assessing the prognosis of children with hydrocephalus [4, 5]. Video recording – EEG monitoring during sleep of children with hydrocephalus allows to detect subclinical epileptic seizures, determine the presence of electrical status of slow-wave sleep (ESES) and calculate the spike-wave index (SWI-index), which can predict the degree of cognitive deficit [6-10]. It has been proven that the presence of ESES contributes to a significant regression of cognitive skills and leads to severe cognitive deficits [10- 16]. It was found that early surgical treatment of progressive hydrocephalus with the establishment of the cerebrospinal fluid shunt system can improve the prognosis of psycho-motor development of children, and the presence of repeated revisions of the shunt correlates with the difficulty of psycho-motor development of children [10-12]. The purpose of our study was to assess the psycho-motor development of children with hydrocephalus and epilepsy; identify the relationship between electrophysiological, radiological and clinical data of children with hydrocephalus to assess the prognosis of cognitive and motor development Materials and methods. Children with unilateral and bilateral ventriculomegaly were included in this study. 71 children were examined retroactively and prospectively on the basis of the Transcarpathian ODL for 3 years (from 2018 to 2021). These diagnoses were confirmed by ultrasound (neurosonography) and neuroimaging (MRI of the brain 1.5 Tesla, MSCT GM). The presence of epileptic seizures was confirmed with the help of EEG monitoring video data using the international model of electrode application "10-20" and evaluation of the electroencephalogram in 3 installations: "common average", "double banana", "transversal". EEG recordings were performed in the active state of children and during sleep. The average sleep duration is 2.5 hours. All patients underwent a trial with photostimulation. 43% of children were tested for hyperventilation. Electroencephalogram was performed in patients every 3 months for 3 years. A total of 620 EEG monitoring was performed over 3 years. Patients are divided into 2 groups: group A – children with progressive hydrocephalus and epilepsy; group B – children with progressive hydrocephalus without epilepsy. Surgical treatment of hydrocephalus with the establishment of the cerebrospinal fluid shunt system was performed in 31 patients with progressive hydrocephalus. Cognitive and motor development was assessed in all patients with hydrocephalus and epilepsy using the MMSE (The Mini-Mental State Examination) age and GMFCS (Gross Motor Function Classification System) scales. Results. The average age of patients in group A was 6 months, in group B – 2.2 years. The sex ratio in group A was 65% / 35% (20 boys / 11 girls), in group B – 80% / 20%, respectively (32 boys / 8 girls). Assessment of cognitive development of patients according to the modified MMSE scales revealed the following changes: In group A (31 patients with hydrocephalus and epilepsy): - normal cognitive development was found in 5 children; - slight delay in cognitive development was found in 9 children; - moderate delay in 12 patients; - severe cognitive deficits in 7 patients. The relationship between electroencephalogram changes and the severity of cognitive deficit was revealed. In children with hydrocephalus, in whom the electrical status of sleep was detected according to the data of long-term EEG monitoring data, a significant deterioration of the data of cognitive level assessment according to MMSE scales was observed. The worst indicators of cognitive development of children with hydrocephalus were found in children with SWI index more than 90%. Assessment of motor skills revealed the following: the ability to walk without additional means of transportation (GMFCS ≤ 2) was found in only 9 children out of 31 patients with hydrocephalus and epilepsy. Other patients had limited mobility: 12 children with hemiparesis (GMFCS> 2, GMFCS> 3), 7 children with lower paraparesis (GMFCS> 4) and 3 children with spastic tetraplegia (GMFCS = 5). Surgical treatment of hydrocephalus with the establishment of the cerebrospinal fluid shunt system was performed in 28 patients with progressive hydrocephalus and epilepsy. A link between repeated shunt revisions and poor cognitive and motor prognosis in patients with hydrocephalus has been identified. Severe postoperative ventriculomegaly with subsequent shunt revisions is associated with an unfavorable prognosis (Evans index> 0.37; odds ratio: 0.16, P = 0.03). In group B (40 patients with hydrocephalus without epileptic seizures) the following changes were detected: - normal cognitive development was found in 25 children; - slight delay in cognitive development was found in 9 children; - moderate delay in 6 patients; - severe cognitive deficits were not detected in any patient in this group. The relationship between the data of long-term EEG monitoring and the state of cognitive development of children with hydrocephalus was revealed. The presence of subclinical seizures during sleep and electrical sleep status were registered in 6 patients from group B. The SWI index correlated in the range from 85 to 90%. These children had cognitive deficits of moderate severity. In children with no pathological changes according to EEG data, no negative prognosis was found in the cognitive development of children with hydrocephalus. Assessment of motor abilities revealed the following: the ability to walk without additional means of transportation (GMFCS ≤ 2) was found in 36 children with hydrocephalus who did not have epileptic seizures. Other patients had limited mobility: 4 children were observed with hemiparesis (GMFCS> 2, GMFCS> 3). Children with severe mobility limitations (GMFCS> 4 GMFCS> 5) were not detected in group B. Assessment of motor abilities revealed the following: the ability to walk without additional means of transportation (GMFCS ≤ 2) was found in 36 children with hydrocephalus who did not have epileptic seizures. Other patients had limited mobility: 4 children were observed with hemiparesis (GMFCS> 2, GMFCS> 3). Children with severe mobility limitations (GMFCS> 4 GMFCS> 5) were not detected in group B. Surgical treatment of hydrocephalus with the establishment of the cerebrospinal fluid shunt system was performed in 3 patients with progressive hydrocephalus from group B. Repeated revisions of the shunt in this group were not detected. Conclusion. Patients with hydrocephalus who have epileptic seizures and electrical sleep status have a worse prognosis in cognitive and motor development. The presence of electrical sleep status with a SWI index of more than 90% contributes to the development of severe cognitive deficits in children with hydrocephalus.
References
Tully HM, Dobyns WB. Infantile hydrocephalus: a review of epidemiology, classification and causes. Eur J Med Genet. 2014;57(8):359–368. doi:10.1016/j.ejmg.2014.06.002 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4334358/.
Munch TN, et al. Familial aggregation of congenital hydrocephalus in a nationwide cohort. Brain. 2012;135(Pt 8):2409–15. [PubMed] [Google Scholar].
Sato O1, Yamguchi T, Kittaka M, Toyama H. /Hydrocephalus and epilepsy./ Childs Nerv Syst. 2001 Jan;17(1-2):76-86.
Anna-Liisa Saukkonen Electroencephalographic findings in hydrocephalic children prior to initial shunting Child’s Nerv Syst (1988) 4:339-343
Gupta N, Park J, Solomon C, Kranz DA, Wrensch M, Wu YW. Long-term outcomes in patients with treated childhood hydrocephalus. J Neurosurg 2007;106:334–9.
Mori K, Shimada J, Kurisaka M, Sato K, Watanabe K. Classification of hydrocephalus and outcome of treatment. Brain Dev 1995;17:338–48 6. Vinchon M, Baroncini M, DelestretI. Adult outcome of pediatric hydrocephalus. Childs Nerv Syst 2012;28:847–54.
Brouwer A, Groenendaal F, van Haastert IL, Rademaker K, Hanlo P, de Vries L. Neurodevelopmental outcome of preterm infants with severe intraventricular hemorrhage and therapy for post-hemorrhagic ventricular dilatation. J Pediatr 2008;152:648–54.
Nelson JS. Principles and Practice of Neuropathology. Oxford University Press, USA. (2003) ISBN:0195125894. https://radiographia.info/article/obstruktivnaya-nesoobshchayushchayasya-gidrocefaliya
Gibbs FA, Gibbs EL (1958) Atlas of electroencephalography. I. Methodology and controls, 3rd edn. Addison- Wesley, Cambridge, Mass 10. Dumermuth G (1972) Elektroencephalographie im Kindesalter. Einftihrung und Atlas, 2nd edn. Thieme, Stuttgart
Bogacz J, Rebello MA (1962) Electroencephalographic abnormalities in nontumor hydrocephalus. Electroencephalogr Clin Neurophysiol 14:123-125
Dr Daniel J Bell and Assoc Prof Frank Gaillard / Hydrocephalus/ https://radiopaedia.org/users/doctordj?lang=us
Charles L. Yeager and John S. Guerrant / Subclinical epileptic seizures – Impairment of Motor Performance and Derivative Difficulties / Calif Med. 1957 Apr; 86 (4): 242–247./ PMCID: PMC151188
Johnson D.L., Contry J. Epileptic Seizure as Cerebrospinal Fluid malfunction // Pediatric Neurosurgery. 1996.24.223-228. — https://www.karger.com/Article/Abstract/121043.
Dincer A, Ozek MM. Radiologic evaluation of pediatric hydrocephalus. Childs Nerv Syst. 2011;27(10):1543–62. doi: 10.1007/s00381-011-1559-x. [PubMed] [CrossRef] [Google Scholar]
Pople IK. Hydrocephalus and shunts: what the neurologist should know. J Neurol Neurosurg Psychiatry. 2002;73(Suppl 1):i17–22. [PMC free article] [PubMed] [Google Scholar]
Hughes JR. A review of the relationships between Landau-Kleffner syndrome, electrical status epilepticus during sleep, and continuous spike-waves during sleep. Epilepsy Behav. 2011;20:247–53.
Veggiotti P, Beccaria F, Papalia G, Termine C, Piazza F, Lanzi G. Continuous spikes and waves during sleep in children with shunted hydrocephalus. Childs Nerv Syst. 1998;14:188–94. [PubMed] [Google Scholar]
Ben-Zeev B, Kivity S, Pshitizki Y, Watemberg N, Brand N, Kramer U. Congenital hydrocephalus and continuous spike wave in slow-wave sleep: A common association? J Child Neurol. 2004;19:129–34. [PubMed] [Google Scholar]
Battaglia D, Acquafondata C, Lettori D, Tartaglione T, Donvito V, Staccioli S, et al. Observation of continuous spike-waves during slow sleep in children with myelomeningocele. Childs Nerv Syst. 2004;20:462–7. [PubMed] [Google Scholar]
Battaglia D, Pasca MG, Cesarini L, Tartaglione T, Acquafondata C, Randò T, et al. Epilepsy in shunted posthemorrhagic infantile hydrocephalus owing to pre- or perinatal intra- or periventricular hemorrhage. J Child Neurol. 2005;20:219–25. [PubMed] [Google Scholar]
Caraballo RH, Bongiorni L, Cersósimo R, Semprino M, Espeche A, Fejerman N. Epileptic encephalopathy with continuous spikes and waves during sleep in children with shunted hydrocephalus: A study of nine cases. Epilepsia. 2008;49:1520–7.
Gupta N, Park J, Solomon C, Kranz DA, Wrensch M, Wu YW. Long-term outcomes in patients with treated childhood hydrocephalus. J Neurosurg 2007;106:334–9
Futagi Y, Suzuki Y, Toribe Y, Nakano H, Morimoto K. Neurodevelopmental outcome in children with posthemorrhagic hydrocephalus. Pediatr Neurol 2005;33:26
Hoppe-Hirsch E, Laroussinie F, Brunet L, Sainte-Rose C, Renier D, Cinalli G, et al. Late outcome of the surgical treatment of hydrocephalus. Childs Nerv Syst 1998;14:97–9.
