Abstract
While the neuropsychological profile for individuals with Spina Bifida (SB) can vary, often certain patterns of strengths and weaknesses are evident across the lifespan. Understanding variability related to neural structure, genetics, ethnicity, and the environment is key to understanding individual differences in outcomes and can be vital in planning interventions and tracking progress. This article outlines the SB Guideline for the Neuropsychological Care of People with Spina Bifida from the 2018 Spina Bifida Association’s Fourth Edition of the Guidelines for the Care of People with Spina Bifida and acknowledges that further research in SB neurocognitive profiles is warranted.
Keywords
Introduction
Neuropsychological studies show a pattern of streng-ths and weaknesses involving motor, cognitive, academic, and adaptive functions in individuals with Spina Bifida [1, 2, 3]. This pattern is most commonly seen among individuals with Spina Bifida who are born with an open spinal lesion (myelomeningocele) and usually have a Chiari II malformation and other congenital brain malformations involving the cerebellum midbrain, and corpus callosum [4]. Most of the existing literature is based on patients who had hydrocephalus treated with surgical implantation of a shunt; however, the literature is just emerging on younger populations with myelomeningocele treated for hydrocephalus with different interventions, such as endoscopic third ventriculostomies Prenatal surgery is also preventing hydrocephalus and the need for shunting in some patients. It remains to be seen whether these different treatment modalities are associated with different neurocognitive profiles.
It is important to identify this subgroup of patients with myelomeningocele, which makes up 9% of the population with Spina Bifida. Individuals born with other types of Spina Bifida do not have the changes in neuroanatomical development referred to above and often have more typical cognitive development [5]. The Spina Bifida Myelomeningocele (SBM) neurocognitive pattern involves strengths in learning skills and performing tasks that rely on associative, rule-based processing (e.g., math fact retrieval, word reading), and weaknesses when learning and performance involves the construction or integration of information (e.g., math problem-solving, reading comprehension) [2].
To illustrate, children with SBM have difficulty with controlled motor performance tasks that require adaptive matching of a motor response to changing visual information which involves the cerebellum [2], and is associated with the Chiari II malformation. However they can learn motor skills through repetition and correction of errors [6, 7, 8, 9, 10] which involves the relatively preserved basal ganglia [4].
In language and reading areas, vocabulary, grammar, and word recognition are strengths [11]. However, children with SBM experience challenges in listening and reading comprehension, and in oral discourse involving the use of language in context (pragmatics) [12, 13, 14]. This has been linked to anatomic changes in the corpus callosum [15].
In mathematics, children with SBM can learn math facts; however, complex procedures that require multiple steps and algorithms are an area of challenge. They often experience difficulties with estimating quantities and have impaired math problem-solving skills [16, 17, 18]. Problems with math a longterm predictor of adult independence, are common in adults and children with SBM [2, 19].
Many children with SBM meet criteria for Attention Deficit/Hyperactivity Disorder, Predominantly Inattentive Presentation (ADHD) [20, 21]. However, in contrast to children with developmental forms of ADHD related to self-regulation, the attention profile of children with SBM is characterized by under-arousal and excessive persistence in controlling attentional focus. These difficulties in alerting and orienting to external stimuli are related to disruptions in midbrain and posterior cortex and are discernable from infancy [22, 24]. It is more appropriate to conceptualize attention deficits, for patients with SBM, as involving posterior brain pathways; this is in contrast to the “executive dysfunction” model, such as with developmental ADHD, traumatic brain injury, and other disorders involving frontal lobe functions.
Despite the modal neuropsychological SBM profile presented above, there is a great deal of variability in neuropsychological outcomes. Understanding the variability in neuroanatomic anomalies, ethnicity, and the environment (socio-economic status and education) is key to understanding individual (rather than group) differences in outcomes. Neurological status, including more severe hydrocephalus, repeated shunt malfunctions, and ethnicity predict poorer outcomes and deviation from the modal profile [5]. Individuals with higher lesion levels have more severe neuroanatomic brain malformations and higher rates of intellectual disability. Spinal defects at T12 and above are more frequent among individuals of Latinx ethnicity, likely related in part, to genes involved in folate metabolism [5, 25]. These populations also are often economically disadvantaged, with diminished access to care and adverse outcomes attributable to social determinants of health, further increasing risk for negative neuropsychological outcomes [5]. These disadvantaged children may not display the aforementioned relative strengths in language and academics that are more typical for children with SBM with lower level lesions and equitable socio-economic circumstances.
Guidelines, goals and outcomes
The goals of the neuropsychology guidelines were both practical and aspirational. Although neuropsychological assessment is clearly indicated for most patients born with SBM, barriers to care include limited access to clinicians with experience in the evaluation of complex medical patients and access to resources (and/or adequate insurance coverage). This process was initiated through the creation of several goals and desired outcomes:
Clinical questions that informed the neuropsychology guidelines
Clinical questions that informed the neuropsychology guidelines
Primary
Optimal development of language academic, and other learning skills. Optimal performance in school, university, and vocational settings.
Secondary
Maximize independence according to individual capabilities. Maximize participation in society.
Tertiary
Acquisition of a job. Utilization of learning skills is apparent in a variety of contexts.
Neuropsychology guidelines
The process of the guideline development was set by the Executive Committee created by the Spina Bifida Association of America (SBA). It included a mix of providers who have worked with patients who have Spina Bifida throughout their careers as well as SBA professionals. The process began with a level 1 review of the literature, updated to include studies that were published between 2002 through 2015, which resulted in the review of 2449 abstracts; these were then forwarded to the level 2 review that resulted in 874 full text articles being archived for working groups. Working groups then reviewed the literature that was forwarded to each committee, and were able to add and subtract research articles based upon their contribution to the field. The full guidelines then included 803 articles; the neuropsychology working group cited 4 articles in their guidelines. The teams worked to craft goals and potential outcomes, along with specific clinical questions for each of the six age groups (Table 1), and then to systematically evaluate the literature’s documentation of the ‘answers’ to the clinical questions. Following peer review by two sets of colleagues, including those in fields working in close collaboration with neuropsychology (e.g., Neurosurgery, Psychology, Transition, and Family Functioning groups) and a broader set of multidisciplinary colleagues, the final version of the guidelines was published in 2018 [26]. The full methodology followed by the working group for writing these guidelines was described by Dicianno et al. [27].
Results
Using the existing literature, as well as our own clinical consensus, the guidelines were developed (Table 2). They document that neuropsychological assessment is indicated throughout the lifespan. Key developmental guidelines included early elementary school in order to identify changes in learning; and the transition out of high school to assess for independent functioning levels.
Although there is often a typical profile of strengths and weaknesses, there is variability in the profile and level of severity of neuropsychological functioning. In addition, multiple factors, including health status and medical history, as well as family structure and access to intervention, impact both the acquisition of skills over time and overall adaptation. The guidelines therefore recommend neuropsychological consultation, monitoring, and evaluations throughout the lifespan.
Following the review of the literature and the creation of the guidelines, there were still some unanswered clinical questions that support the need for ongoing research and updating of guidelines in the future. Additional research was considered essential given the changes in neurosurgical care that are currently occurring with prenatal surgery and endoscopic third ventriculostomy and choroid plexus cauterization procedures (ETV/CPC) procedures. However, the need for additional research on the aging brain was also highlighted.
Discussion
The SBA Guidelines for the Neuropsychological Care of People with Spina Bifida recommend neuropsychological evaluation at key times to identify strategies for learning and improve outcomes for independent functioning. Evaluation is also recommended in order to better delineate individual variations in the SBM modal profile. Lastly neuropsychological assessment is recommended in order to better understand impact of new neurosurgical interventions.
Early childhood
Understanding the basis for strengths and weaknesses in SBM and using that information to inform interventions may prevent some of the negative outcomes. Fletcher et al. [3] suggest four areas that may be important for facilitating the early development of children with SBM, including (a) early movement, with a focus on encouraging the child to initiate and respond to environmental contingencies that require action [7]; (b) early language, to ensure development not only of vocabulary and literal language skills, but the child’s sensitivity to contextual and pragmatic aspects of language [12, 31] (as language develops, it is also important that the child uses language flexibly to develop connections and relationships among events and objects in their environment, and not to simply describe them); (c) early attention and social problem solving, with a focus on establishing contingencies that link action and movement [7, 28]; and (d) responsive parenting, which represents strategies that support the development of skills in at-risk children [6, 29]. Families with higher expectations for autonomy may be more likely to promote the flexible use of language, stronger attention, and independent movement early in development [29].
Later childhood
Many of the later developmental needs of the child with SBM involve school and learning. As a general principle, the approach to intervening in any area that involves school or behavior does not necessarily deviate because the child has SBM. Because there is little research specific to the learning needs of children with SBM, the working principles are that these children will benefit from interventions specific for their cognitive and academic difficulties, such as those for reading comprehension or math problem solving. These have been shown to be effective in other populations, such as children with learning or attention disorders [40], and which have, on a small scale, been shown to be effective for children with SBM [39]. One of the reasons that interventions for struggling students might be applicable is that many interventions are explicit in terms of identifying goals, providing external organizational structures to build skills in a step by step fashion (“scaffolding skills”), and teaching strategies directly by using associative learning to enable assembled processing.
Modal profile and individual variation
Understanding SBM requires that we identify the modal profile for outcome in a number of domains and then sculpt that outcome according to specific factors that we know produce individual variations in the profile. As we learn more about both group outcomes and individual function, we will be able to identify the best possible interventions based on information from both individual and group outcomes. The SBM profile, both modal and individual, is quite distinctive and is not captured simply by assigning these children to categories such as ADHD, nonverbal or right hemisphere learning disability, or a dysexecutive syndrome. Even though SBM shares some features with each of these conditions, and at a broad level such terms may facilitate communication around the modal profile, SBM is not well characterized by any of them. Assignment of any of these diagnostic labels in no manner dictates effective interventions. What is more important is accurately conceptualizing an individual’s strengths and weaknesses in a way that enables them to receive services and to help guide the nature and content of such services.
Further research
Development of these guidelines also raised several questions that were not answered through a review of the existing published literature and which we identified as domains for further research. To what extent can the early use of Magnetic Resonance Imaging (MRI) findings (e.g., malformations, dysplasia, reduced volume, and agenesis) predict domains of risk and identify potential early interventions to support development? What specific interventions in infancy are most successful in supporting the development of motor, cognitive, early literacy and numeracy skills? Multiple questions about shunt management have been raised, including those related to how the earliest time periods are managed in infants. The research has yet to detail the longterm effect of sequential monitoring of hydrocephalus on development. For example, is it better to shunt early and control hydrocephalus or to monitor ventricular expansion over time, and to identify the best indicators of the need for shunt diversion?
Also, there are still questions about how to manage some of the cognitive challenges that have been documented for many patients with Spina Bifida. One question is whether and to what extent different interventions used across the lifespan involving cognition, learning, and social skills are effective for persons living with Spina Bifida. Another is whether attention problems are best treated from pharmacological and/or non-pharmacological perspectives, as this has not been explored through randomized trials.
In addition, there are open questions with respect to the effects on neuropsychological function of recent changes in treatment for hydrocephalus, including prenatal repair in the Management of Myelomeningocele Study (MOMS) and the ETV/CPC procedures. There is a need for research to indicate how these treatments affect the health and physical and neurocognitive development of infants and children over time. The first report of school-age outcomes from the MOMS trial showed an improvement in motor functions and quality of life and a reduction of parental stress, but little evidence for improvement in cognitive functions and adaptive skills [42]. Furthermore, while many children who have undergone ETV/CPC procedures are still young, they may also demonstrate improvements over the more typical outcomes documented for those who were shunted in the past. Given increasing survival of individuals with SB into middle and later adulthood, the working group also noted a lack of information on the effects of SB and hydrocephalus on brain and neuropsychological functioning in middle and later adulthood.
The SB Guidelines for the Neuropsychological Care of People with Spina Bifida from the SBA’s Fourth Edition of the Guidelines for the Care of People with Spina Bifida are based on significant advances in knowledge regarding both the modal neurocognitive profile of Spina Bifida as well as individual differences in that profile related to variability in neural structure, genetics, ethnicity, and the environment. Patterns of neuropsychological strengths and weaknesses that are evident in many individuals with Spina Bifida are discernable early in development and across the lifespan. Understanding the common neuropsychological profiles as well as individual differences in outcomes is critical for planning interventions at all ages and for tracking progress. Recognition of the specific aspects of the cognitive profile will also help medical providers to better understand how to work with their patients more successfully to facilitate their independent functioning over time. Despite considerable advances in understanding neuropsychological processes and outcomes in Spina Bifida, there is clearly need for further research on: 1) the effects of neurosurgical, pharmacological, neurobehavioral, and academic interventions on neuropsychological outcomes; and 2) the effects of Spina Bifida on the aging brain and ways to promote brain health in middle to later adulthood.
Footnotes
Acknowledgments
This edition of the Journal of Pediatric Rehabilitation Medicine includes manuscripts based on the most recent “Guidelines For the Care of People with Spina Bifida,” developed by the Spina Bifida Association. Thank you to the Spina Bifida Association for allowing the guidelines to be published in this forum and making them Open Access.
The Spina Bifida Association has already embarked on a systematic process for reviewing and updating the guidelines. Future guidelines updates will be made available as they are completed.
Executive Committee
Timothy J. Brei, MD, Spina Bifida Association Medical Director; Developmental Pediatrician, Professor, Seattle Children’s Hospital Sara Struwe, MPA, Spina Bifida Association President & Chief Executive Officer Patricia Beierwaltes, DPN, CPNP, Guideline Steering Committee Co-Chair; Assistant Professor, Nursing, Minnesota State University, Mankato Brad E. Dicianno, MD, Guideline Steering Committee Co-Chair; Associate Medical Director and Chair of Spina Bifida Association’s Professional Advisory Council; Associate Professor, Department of Physical Medicine and Rehabilitation, University of Pittsburgh School of Medicine Nienke Dosa MD, MPH, Guideline Steering Committee Co-Chair; Upstate Foundation Professor of Child Health Policy; SUNY Upstate Medical University Lisa Raman, RN, MScANP, MEd, former Spina Bifida Association Director, Patient and Clinical Services Jerome B. Chelliah, MD, MPH, Johns Hopkins Bloomberg School of Public Health
Additional acknowledgements
Julie Bolen, PhD, MPH, Lead Health Scientist, Rare Disorders Health Outcomes Team, National Center on Birth Defects and Developmental Disabilities, Centers for Disease Control and Prevention Adrienne Herron, PhD Behavioral Scientist, Intervention Research Team, National Center for HIV/AIDS, Viral Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention Judy Thibadeau, RN, MN, Spina Bifida Association Director, Research and Services; former Health Scientist, National Spina Bifida Program, National Center on Birth Defects and Developmental Disabilities, Centers for Disease Control and Prevention
Funding
The development of these Guidelines was supported in part by Cooperative Agreement UO1DD001077, funded by the Centers for Disease Control and Prevention. Its contents are solely the responsibility of the authors and do not necessarily represent the official view of the Centers for Disease Control and Prevention or the Department of Health and Human Services.
Conflict of interest
The authors have no conflict of interest to report.