Neuropsychological profiles in children and young adults with spina bifida

Spina bifida (myelomeningocele) is one of the most complex birth defects compatible with life, with an estimated prevalence between 3.06 and 3.13 cases per 10,000 live births [1].

Myelomeningocele is the most common form of “spina bifida,” but other forms of open and closed lesions exist, including lipomyelomeningocele, diastematomyelia, diplomyelia, myelocystocele, myeloschisis, and fatty filum [2]. Spina bifida is the most common central nervous system birth defect encountered by the pediatric neurosurgeon. It is defined by characteristic development abnormalities of the vertebrae and spinal cord and associated changes in the cerebrum, brainstem, and peripheral nerves. As a result of denervation, muscle imbalance ensues and can result in abnormalities at the hip, knee, and foot. Anesthesia of various portions of the skin can lead to pressure sores, particularly later in life. Anorectal neuropathy may cause a variety of defecatory dysfunctions. Urologic abnormalities are also common. These multisystem abnormalities associated with spina bifida contribute to its widely accepted identity as the most complex development defect compatible with long life [3]. With advances in medical care, more individuals with spina bifida are surviving to adulthood [4, 5]. A total of 43 Italian children, aged between 6 and 16 years, diagnosed with spina bifida, myelomeningocele, and shunted hydrocephalus, followed in Spina Bifida Centre of Policlinico Universitario A. Gemelli – Roma, have been described clinically and completed a neuropsychological battery in order to evaluate their profile.

A total of 43 Italian children and young adults diagnosed with spina bifida completed a neuropsychological assessment battery in order to have their profiles evaluated. Enrolled children underwent cognitive assessment by means of the Weschler WISC-IV cognitive test and assessment of the attention sustained through the LEITER test. In addition, parents were asked, in order to obtain a personality and behavior profile of the children, to fill in a “CBCL 6-18 years” questionnaire and to fill in a Barthel Index questionnaire. Informed consent was signed by the parents. The protocol for this study was approved by the Ethics Committee of the Fondazione Policlinico A. Gemelli IRCCS, ID number: 3218 (2020).

A total of 43 patients, 22 females (51.2%) and 21 males (48.8%), have been enrolled in the study. Mean age of the whole sample was 10.72 years (±3.1) with a minimum age of 6 years and a maximum age of 16. As shown in Table 1, the majority of our patients completed primary school (21, 48.8%) and received a lipoma diagnosis (22, 51.2%) or a myelomeningocele (MMC) (20, 46.5%) or a lipomyelomeningocele (LMMC) diagnosis (1, 2.32%). Hydrocephalus is present in 16 patients (37.2%) and all of them have been diagnosed as myelomeningocele. Ventriculoperitoneal shunt is present in 14 patients (32.6%). Most of the patients were in a condition of autonomous gait (26, 60.5%). Barthel Index mean value was 14.91 (±5.1). Table 2 shows that WISC mean value was 88.83 (±19.1) and, in more detail, the Verbal Comprehension Index mean value was 96.58 (±16.7), the Working Memory mean value was 83.56 (±18.6), and the Processing Speed Index mean value was 90.93 (±17.6). The distributions of categorical variables by gait highlighted a statistically significant difference in Barthel Index (p = 0.001) where patients with wheelchair presented the lowest Barthel Index mean value (8.3±4.6) and the highest was presented by autonomous patients (17.1 ± 3.1). Also, the Processing Speed Index of the WISC-IV QI scale was statistically significant (p = 0.027), with the highest value presented by autonomous patients (95.8 ± 12.8) and the lowest by patients using a wheelchair (75.5 ± 19). See Table 3 for details. Table 4 presents the comparisons of patients according to diagnosis. WISC-IV QI mean value is 98 (±15.7) for lipoma patients and 78.7 (±17.6) for LMMC and MMC patients (p = 0.001). In more detail, Perceptual Reasoning (p < 0.0005), Working Memory (p = 0.01), and Processing Speed index (p = 0.001) highlighted a significant difference between the groups. The attention sustained subscale of the LEITER presented a mean of 6.9 (±3.1) for lipoma patients and a men value of 4.6 (±3.1) for LMMC and MMC patients (p = 0.024). Table 5 reports a comparison between patients with and without hydrocephalus about cognition and autonomy. As shown, patients with hydrocephalus had worse cognition score regarding IQ (p < 0.001) and autonomy (Barthel Index) (p < 0.001).

Bivariate analyses have shown that within those who are autonomous, there are no significant differences between lipoma and MMC patients in terms of neuropsychological test results, similarly among wheelchair users and among tutor users.

There is no statistically significant difference, for neuropsychological tests result, comparing patients without hydrocephalus and with different gait abilities. However, within patients with hydrocephalus, some tests gave significantly different results between gait ability groups: The Barthel Index shows significantly different results between “autonomous vs. wheelchair” (p = 0.035) and “tutor vs. wheelchair” (p = 0.017). Perceptual reasoning presented significantly different results between “autonomous vs. wheelchair” (p = 0.042) and “tutor vs. wheelchair” (p = 0.013). Processing speed was significantly different between “autonomous vs. wheelchair” (p = 0.033) and “tutor vs. wheelchair” (p = 0.031). LEITER attention sustained presented significantly different results between “autonomous vs. wheelchair” (p = 0.024) and “tutor vs. wheelchair” (p = 0.049). See Table 6 for details.

Spina bifida malformation (SBM) is a neural tube defect originating in the first 30 days of gestation and associated with failure of the caudal end of the neural tube to close. It is a heterogeneous congenital disorder with complex physical and neuropsychological symptomatology. It is associated with developmental anomalies of both the spine and the central nervous system. Different forms of spina bifida can be distinguished from mild to severe. The most common form is myelomeningocele (MMC). Most patients with myelomeningocele present associated hydrocephalus. Hydrocephalus in SBM results from the Chiari II cerebellum and hindbrain malformations, which obstructs the flow of the cerebrospinal fluid (CSF) at the level of the third and fourth ventricles. Surgical management with ventriculoperitoneal shunt implantation (VPS) is a widely used, effective treatment for hydrocephalus. However, consistent follow-up is necessary after VPS, taking into consideration several shunt-related complications including obstruction, fracture, and infection. Also, the endoscopic third ventriculostomy (ETV) procedure is well recognized as an effective alternative to cerebrospinal fluid (CSF) shunt placement and has been the ideal treatment of choice for obstructive hydrocephalus in recent years. As for the neurocognitive aspects, children with hydrocephalus and SBM are more impaired in spatial, math, memory, and concept formation domains, compared to their relative strengths in vocabulary and word reading domains [6, 7]. Within content domains, cognitive strengths involve the learned association and categorization of stimulus information, such as word recognition, vocabulary, and priming abilities. Areas of weakness involve abstract assembly and construction of information, such as coordinating visual perception, mathematical computation, reading and language comprehension, and concept formation tasks [6‐8]. The purpose of this study was to observe the psychological and neuropsychological condition of children affected by spina bifida, a condition with a great severity and clinical variety. The study showed that lipoma patients have a more adequate cognitive function development than MMC patients. Moreover, patients with autonomous ambulation (most of them are lipoma patients) presented a normal cognitive development unlike patients in need of a wheelchair or a tutor. Patients that need a wheelchair are the most affected both clinically and cognitively. Considering the components of cognitive processes (WISC-IV), such as Perceptual Reasoning, Working Memory, and Processing Speed Index, the study proved that these skills are preserved in lipoma patients rather than in MMC patients who have difficulties in these skills due to the severity of their pathology. Particularly, the Processing Speed ability is linked with concentration and attention, cognitive flexibility, visual ability, and organizing an autonomous task fast. These results can be useful in planning dedicated therapeutic protocols such as suitable rehabilitation treatments, speech therapy, psychomotor skills, and cognitive enhancement. Cognitive ability scores, such as Working Memory (WISC-IV) and Sustained Attention (LEITER), are in both lipoma and LMMC and MMC patients below normal values and/or slightly below normal values [9, 10].

From a behavioral point of view, the analysis of the questionnaires filled by the parents highlights that no clinical or pathological scores are present in the three scales investigated by the CBCL tool. Results highlight that children, even if they do not have clinical scores, tend to use internalizing defense mechanisms, showing an attitude characterized by greater emotional closure and social withdrawal rather than externalizing attitude (outbursts or aggression).

Study’s results highlighted that children with spina bifida, checked from birth constantly each 6-12 months, have a normal cognitive functioning characterized by difficulties in working memory, which is slightly lower than the normal value, but with a strength in verbal understanding. These findings can guide a better assessment of patients’ needs in order to develop prevention protocols (suitable rehabilitation treatments such as speech therapy, psychomotor skills, cognitive enhancement) particularly tailored for children with hydrocephalus who appear to have the more deficient skills. About the presence of hydrocephalus, the authors observed that these patients have worse score both for cognitive intelligent quotient analyzed with the WISCH scale and for autonomy with the Barthel Index. These results can be explained because patients with hydrocephalus have severe clinical manifestations of spina bifida and also because hydrocephalus causes a worse impact on quality of life and cognitive performances.

This study underlined that spina bifida patients should also be evaluated for their neuropsychological deficits in order to organize specific rehabilitation programs.