Role of child neurologists and neurodevelopmentalists in the diagnosis of cerebral palsy

Abstract

Objective

To contextualize the role of child neurologists and neurodevelopmentalists (CNs/NDDs) in cerebral palsy (CP) care, we review the changing landscape of CP diagnosis and survey stakeholder CNs/NDDs regarding their roles in CP care.

Methods

The optimal roles of the multiple specialties involved in CP care are currently unclear, particularly regarding CP diagnosis. We developed recommendations regarding the role of CNs/NDDs noting (1) increasing complexity of CP diagnosis given a growing number of genetic etiologies and treatable motor disorders that can be misdiagnosed as CP and (2) the views of a group of physician stakeholders (CNs/NDDs from the Child Neurology Society Cerebral Palsy Special Interest Group).

Results

CNs/NDDs felt that they were optimally suited to diagnose CP. Many (76%) felt that CNs/NDDs should always be involved in CP diagnosis. However, 42% said that their patients with CP were typically not diagnosed by CNs/NDDs, and 18% did not receive referrals to establish the diagnosis of CP at all. CNs/NDDs identified areas of their expertise critical for CP diagnosis including knowledge of the neurologic examination across development and early identification of features atypical for CP. This contrasts with their views on CP management, where CNs/NDDs felt that they could contribute to the medical team, but were necessary primarily when neurologic coexisting conditions were present.

Discussion

Given its increasing complexity, we recommend early referral for CP diagnosis to a CN/NDD or specialist with comparable expertise. This contrasts with current consensus guidelines, which either do not address or do not recommend specific specialist referral for CP diagnosis.

Cerebral palsy is the most common cause of disability in childhood, affecting 2–3 of every 1,000 live births.^1–3 Its presentations are diverse involving multiple possible motor manifestations (including motor delay, spasticity, dystonia, chorea, ataxia, and hypotonia) and associated comorbidities (including cognitive impairment, autism, epilepsy, pain, and difficulties with vision, communication, feeding, and sleep).^4,5 Its etiologies can range from temporally isolated injuries (e.g., periventricular leukomalacia due to prematurity) to structural brain malformations (e.g., lissencephaly) to genetic etiologies without obvious structural brain malformations (e.g., chromosomal deletions or duplications).^6–8 Noting its protean presentation and systemic involvement, the combined efforts of multiple medical specialties are necessary for CP care. This list includes, but is not limited to, neurologists, neurodevelopmentalists, general pediatricians, developmental pediatricians, physical medicine and rehabilitation specialists, orthopedic surgeons, neurosurgeons, and physical, occupational, and speech therapists who are all variably considered to be the primary provider for an individual with CP.⁹ Each of these specialties contribute unique areas of expertise that to the diagnosis and management of patients with CP.

However, it is unclear what the optimal roles of each of these specialties might be in the care of those with CP. This is most apparent with regard to CP diagnosis. Current recommendations suggest that making a diagnosis of CP can be within the purview of the primary care provider and referral to a specialist is only necessary if questions remain.¹⁰ Therefore, general pediatricians most commonly make the diagnosis of CP, and child neurologists or neurodevelopmentalists (CNs/NDDs) may only be involved in CP diagnosis in less than one-quarter of patients.¹¹

A systematic review of the evidence has led to guidelines for early CP diagnosis when clear risk factors (like prematurity or neonatal hypoxic-ischemic encephalopathy) are discoverable in the neonatal period.¹² When these risk factors are absent, it has been recently suggested by international consensus that referral to a specialist should be made early for potential CP diagnosis at the first signs of motor delay.¹³ However, in both scenarios, it remains unclear which specialist with which skill set is optimally suited to make the most timely and accurate CP diagnosis.

The skills necessary to make a CP diagnosis have become increasingly broad. There is growing recognition of genetic etiologies for a CP phenotype, which have implications for family counseling, screening of comorbidities, anticipatory guidance, and long-term prognosis.¹⁴ There has also been an increased recognition of atypical or progressive disorders that can be confused for CP particularly early in life (the so-called CP mimics), many of which require early recognition and initiation of treatment to prevent long-term sequelae (table 1).^15–17 Identifying CP etiologies and distinguishing them from CP mimics is a critical but nuanced task. To do this well, the CP diagnostician must have expertise in diagnosing the full spectrum of neurologic conditions that present with a motor disorder.

Table 1.

Examples of genetic cerebral palsy etiologies vs cerebral palsy mimics

CP diagnosis requires identification of a “non-progressive disturbance to the developing fetal or infant brain.”⁸ Therefore, it is critical to elucidate any perinatal or early life history of such a disturbance and correlate this history with the imaging pattern of brain injury. This combined approach can help guide the need for any further testing for genetic CP etiologies or treatable non-CP etiologies. For example, absence of periventricular leukomalacia, residua of intraventricular hemorrhage, or other imaging evidence of compatible brain injury may make a history of prematurity alone insufficient to support a diagnosis of CP in a young child with significant motor delays for corrected age. Therefore, the ideal CP diagnostician should be able to reconcile the perinatal clinical history directly with their interpretation of imaging patterns of injury.

Motor phenotyping can also be critical for accurate CP diagnosis. The majority of children with CP are understood to have spasticity, but other motor disorders are also present in children with CP, including other disorders of tone, hyperkinetic movement disorders, and negative motor signs.^18–23 Noting that many of these motor abnormalities can coexist in the same child with CP, accurate motor phenotyping can be difficult.²⁴ For example, dystonia in CP, despite often being functionally debilitating, may not be diagnosed for years after onset.^25–27 Accurate identification of these motor abnormalities is critical for instituting appropriate treatments but can also be critical for confirming the diagnosis. Children with ataxia, hypotonia, or dystonia-predominant CP are more at risk of developing progressive or additional symptoms that, in time, become incompatible with a diagnosis of CP.²⁸ Identification of rigidity in young children can be virtually pathognomonic for neurotransmitter disorders, many of which are treatable.¹⁵ Therefore, the ideal diagnostician should have motor phenotyping expertise.

Early CP diagnosis in infants with known perinatal risk factors (table 2) is facilitated by the use of infant standardized motor and neurologic assessment scales such as the Prechtl General Movements Assessment or the Hammersmith Infant Neurological Examination.¹² In combination with the correlation of neuroimaging findings with a detailed history regarding potential risk factors for CP, using infant motor scales improves early CP detection before age 5 months.¹² Therefore, the use of these scales should become the standard clinical practice for children known to be at risk of CP (e.g., via a neonatal intensive care unit follow-up clinic).²⁹ Early diagnosis facilitates early intervention, which capitalizes on critical periods of neuroplasticity and minimizes secondary complications related to aberrant musculoskeletal growth and development.¹² In addition, caregivers benefit from early diagnosis for multiple reasons including having a framework to understand their child's symptoms, gaining membership to a community of individuals managing similar symptoms, and gaining early access to ongoing rehabilitation therapies and social services.^11,12,30 Therefore, the ideal diagnostician should be proficient in early CP diagnosis.

Table 2.

Examples of perinatal risk factors for cerebral palsy

With these skills in mind, and noting that early and accurate CP diagnosis should be our goal for every patient, we propose that CNs/NDDs may be well suited to be CP diagnosticians. This is a departure from current clinical practice and consensus guidelines, which either do not mention or do not specify the skill set necessary for early and accurate CP diagnosis, Therefore, to help inform this recommendation, we surveyed a group of CNs/NDDs with special interest in the care of children with CP as evidenced by their involvement with the Child Neurology Society (CNS) Cerebral Palsy Special Interest Group (CP-SIG). We see this as the beginning of a collaborative multidisciplinary discussion between the multiple medical specialties with an interest in CP to explore how we may best complement each other's expertise to ensure optimal care for our shared patients.

Methods

We surveyed CN/NDD attendees of the CNS CP-SIG Meeting on October 25, 2019, at the CNS Annual Meeting in Charlotte, NC. Survey responses were anonymously obtained in 2 parts: (1) using a wireless text and web-based response system (Poll Everywhere, San Francisco, CA) in real time during the SIG meeting with multiple-choice question prompts followed by open discussion and (2) using a REDCap survey link emailed to all SIG meeting attendees with responses collected between February 5 and February 27, 2020.

Standard protocol approvals, registrations, and patient consents

This study was granted a human subjects research exemption from the Washington University School of Medicine Institutional Review Board.

Data availability

Anonymized data will be shared by request from any qualified investigator.

Results

Forty-four CNs/NDDs from the CNS CP-SIG were surveyed, of whom 41 responded to survey questions (93%). CP-SIG attendees were comprised largely of physicians from academic centers (84%) who see patients in both the inpatient and outpatient setting (67%) and who have been in practice for at least 1 year (63%), with 24% in practice for more than 10 years. The vast majority had a dedicated Cerebral Palsy Clinic or Cerebral Palsy Center at their home institution (81%). The majority of respondents (63%) felt that the group should focus on increasing and clarifying the role of CNs/NDDs and another 17% felt that an emphasis should be placed on education around CP diagnosis. Therefore, CP-SIG members represent a select group of clinicians primarily at academic centers focused on the care of children with CP (table 3).

Table 3.

Respondent clinical experience and practice setting

Regarding when CNs/NDDs should be involved in the care of children with CP, the majority felt that they should always be involved before or when making the CP diagnosis (76%). During open discussion during the SIG meeting, elucidating and properly treating other neurologic etiologies of motor disability was cited most often as the reason that CNs/NDDs may be well poised to confer a CP diagnosis. Many advocated for early referral for diagnosis for this reason. However, none felt that workup for these alternate etiologies of motor disability would delay conferring a CP diagnosis if convincing clinical evidence was present. Respondents unanimously felt comfortable with providing a definite or provisional diagnosis of CP at less than 2 years old (table 4 and figure).

Table 4.

Respondent views on the role of child neurologists and neurodevelopmentalists in cerebral palsy care

Figure. Child neurologist and neurodevelopmentalist (CN/NDD) views on their roles in cerebral palsy (CP) care.

*Autism, epilepsy, intellectual disability, dystonia, and medically refractory spasticity; **gross motor function classification system.

Regarding skills that may be important for CP diagnosis, CNs/NDDs felt that they had unique expertise in performing and interpreting the neurologic motor examination across development, early recognition of signs of motor regression, recognition of findings that are atypical for CP (table 5), interpretation of neuroimaging together with correlation to clinical findings, and accurate identification of different motor abnormalities in CP. Of the surveyed skills, CNs/NDDs felt that expertise in the neurologic motor examination, identification of motor regression, and recognition of atypical CP features were critical for CP diagnosis—all skills in which CNs/NDDs felt that they were expert. CNs/NDDs recognized that expertise in infant motor scales was also valuable in CP diagnosis but conceded that they were overall merely competent in their usage (table 6 and figure).

Table 5.

Features atypical for cerebral palsy^15,16,51

Table 6.

Respondent views on the overlap between skills important for cerebral palsy care and the expertise of child neurologists and neurodevelopmentalists

Despite the desire of CNs/NDDs to be involved in CP diagnosis and their perceived expertise in skills necessary for CP diagnosis, they may currently be underused for this purpose. Forty-two percent of CNs/NDDs note that their patients with CP are typically not diagnosed by CNs/NDDs. Only 18% of CNs/NDDs are referred patients for diagnosis before age 1 year, which is recommended for screening for early CP diagnosis. Perhaps more surprising is that 18% of CNs/NDDs are not referred patients for diagnosis at all (table 4 and figure).

Although CNs/NDDs desire a prominent role in CP diagnosis, they had mixed feelings regarding an obligate role in management of patients with CP. Slightly more than half (53%) felt that a CN/NDD should be only be involved with ongoing management in the setting of certain neurologic coexisting conditions (e.g., autism, epilepsy, dystonia, or spasticity that has been refractory to medical management by the referring provider). Only 21% felt that ongoing CN/NDD involvement was always indicated in children with CP regardless of their other associated symptoms. In line with this, 53% of CNs/NDDs primarily manage the care of children with CP at their centers, followed next by physical medicine and rehabilitation medicine (28%). When CP-SIG members were instead asked what subspecialty should be responsible for the managing the care of children with CP, a slightly higher proportion felt that this should be the responsibility of CNs/NDDs (64%) perhaps reflecting a high rate of neurologic coexisting conditions in the children with CP cared for at the respondents' home institutions (table 4 and figure).

Conditional involvement of CNs/NDDs in management of patients with CP was also reflected in their skills self-assessments. CNs/NDDs felt that they had some expertise in almost all skills important for management about which they were specifically asked. However, although CNs/NDDs felt that they had specific expertise in multiple skills required for CP diagnosis, when asked about management, CNs/NDDs only felt that they had unique expertise with regard to epilepsy treatment. Furthermore, although 64% of CNs/NDDs felt that they should primarily manage children with CP at their centers, only 42% felt that CNs/NDDs were specifically qualified to coordinate their care (table 6 and figure).

When asked to include any additional skills they possessed with regard to the care of patients with CP, CNs/NDDs again focused on diagnosis. The most common responses cited the ability to take detailed neurologic histories (15%) and evaluate etiology (15%), including knowing when to send additional testing and what testing to send.

Discussion

Current consensus guidelines do not obligate referral to a CN/NDD for CP diagnosis. Therefore, it is not surprising that the majority of children with CP are not diagnosed by CNs/NDDs.^1,10,11 However, noting the increasing complexity involved in making an early and accurate CP diagnosis, CNs/NDDs may be best suited to be CP diagnosticians. CN/NDD training milestones per the American College of Graduate Medical Education (ACGME) focus on expertise in the neurologic examination across development, diagnosis of multiple potential CP mimics, and neuroimaging interpretation: all skills that are paramount to early and accurate CP diagnosis.^{12,15–17,28} Concomitantly, the surveyed CN/NDD stakeholders agreed that they could provide specific expertise with regard to an accurate assessment of the neurologic examination across development, identification of progressive motor disease, and identification of features atypical for CP (table 5), all of which they identified as skills that were critical for making an early and accurate CP diagnosis. Therefore, the skills self-assessment within this group of CNs/NDDs overlaps nicely with ACGME training milestones, further supporting the specific and optimal role for CNs/NDDs in CP diagnosis.^31,32

Mandating that CNs/NDDs become more responsible for CP diagnosis may be a difficult task, noting the mismatch in the prevalence of CP and the relatively limited availability of CNs/NDDs. However, even in areas with CNs/NDDs specializing in CP (like the areas served by our survey respondents), CNs/NDDs may be underused with regard to diagnosis. Almost 1 in 5 CNs/NDDs surveyed, despite their noted interest in CP care, do not receive any referrals for diagnosis. The majority do not receive referrals for diagnosis until after age 1 year, which is later than the recommended age to make a CP diagnosis.^12,13 Delayed diagnosis results in delayed access to the most affordable therapy services in the United States or elsewhere (e.g., Early Interventions/FirstSteps) which children age out of by 3 years old. These therapies can be particularly valuable if instituted early, and a delayed diagnosis decreases the likelihood of their usage, particularly for families who may not have the means to fund other therapy services.

Recognition of the CP phenotype is the starting point of diagnosis, which must then involve the determination of CP etiology. There are a broad and still growing number of etiologies that can yield a CP phenotype. Determination of the CP etiology is critical for appropriate management, surveillance, prognostication, and counseling for family planning. We propose that there is an important distinction here to be made between what has often been referred to as CP mimics and CP with a nonacquired injury etiology (table 1). CP is purely a clinical descriptor and, as such, is an umbrella term for the clinical phenotype that can result from a broad range of etiologies (including structural malformations and genetic abnormalities).^6,8 Any child with a nonprogressive motor disability from a central etiology should be given a diagnosis of CP.⁸ The term CP mimic has tended to focus on children who may have briefly met phenotypic criteria for CP but then demonstrated a progressive motor phenotype, thus no longer meeting criteria for CP diagnosis (for example, a hypotonic infant born prematurely but with normal imaging who later develops progressive dystonia and is found to have a neurotransmitter disorder).^16,17,33 In contrast, CP with a nonacquired injury etiology encompasses children who truly have a nonprogressive motor disability and therefore continue to meet the definition of CP (for example, a child with bilateral schizencephaly, a pathogenic COL4A1 mutation, nonprogressive spastic quadriparesis, and epilepsy).^34,35 In these children, it is valuable to provide both the diagnosis of CP together with the etiologic descriptor, an area in which CNs/NDDs may be particularly adept.

With regard to early CP diagnosis, all surveyed CNs/NDDs noted that it was possible to make a definite or provisional early CP diagnosis. They additionally felt they had unique expertise in neuroimaging interpretation and correlation with a detailed neurologic history, key evidence-based skills required to make an early CP diagnosis.¹² However, CNs/NDDs also noted that expertise in validated infant motor assessment scales was an area of relative weakness for them. These scales can be administered in the first months of life when discussions about potential CP diagnosis in high-risk infants should begin. Given that infant motor assessment scales have been shown to facilitate early CP diagnosis and intervention, CNs/NDDs may benefit from training in the utility and use of these scales, including incorporating the Prechtl General Movements Assessment into the standard infant neurologic examination.^12,29

CNs/NDDs identified multiple skills as important for management of patients with CP. However, they did not identify any of them as critical, reinforcing that many different specialties with a broad range of skills and training are equally qualified to manage CP. CNs/NDDs felt that they could provide unique expertise only with regard to the management of epilepsy in CP, but felt that they were at least competent and typically well versed with other CP management skills. Although CNs/NDDs agreed that many specialties could manage tone abnormalities in CP, they did indicate particular expertise in accurate tone diagnosis. As appropriate tone and movement disorder diagnosis is required for appropriate management, any difficulty in the management of tone by another provider should prompt referral to a CN/NDD with appropriate expertise to confirm accurate motor phenotyping.

The goal of the CP diagnostic evaluation is to both characterize the CP phenotype and determine the CP etiology, skills in which CNs/NDDs may be particularly adept. We propose that CNs/NDDs may be well suited to be CP diagnosticians based on the available evidence regarding early CP diagnosis,^12,29 CP etiologies and mimics,^14–17 and the difficulties involved in CP motor phenotyping.^24,25,27 The training focus of CNs/NDDs largely supports a role in each of these areas.^31,32 These recommendations are additionally supported by the views of a community of CNs/NDDs who have specific interest in caring for children with CP as evidenced by their involvement with the CNS CP-SIG.

Taking these considerations together, we advocate for early consideration of a CP diagnosis (at least by age 12 months noting that a CP diagnosis is feasible at less than 5 months of age) according to published evidence-based and consensus referral guidelines (table 6).^12,13

We additionally advocate that the diagnosis of CP should be made by a specialist or specialist team who is comfortable with all of the following:

1. Early diagnosis of CP

2. The pediatric neurologic examination across all stages of development

3. Early identification of motor regression

4. Identification of features atypical for CP (table 7)

5. Identification of CP etiologies (table 1).

Table 7.

Clinical features in infants that should prompt referral to a motor disorder specialist for possible cerebral palsy diagnosis (adapted from Novak et al., 2017¹² and Boychuck et al., 2020¹³)

If available within the referral region, CNs/NDDs may be most likely to fit all these criteria.

Our recommendations were informed by a small group of CNs/NDDs interested in CP with a range of backgrounds and expertise (members of the CNS CP-SIG). Although almost a quarter of respondents had been in practice for more than 10 years, over half had been in practice for less than 5 years. That is, our respondents tended to be young, which is ultimately encouraging regarding the future of CNs/NDDs in CP care. We report the CP-SIG's survey responses not as a definitive characterization of the entire field but to delineate the opinions of a core group of individuals who have high exposure to the CP patient population. Although the views of the surveyed CNs/NDDs are confirmatory, our recommendations are primarily supported by evidence-based assessments of the value and feasibility of early and accurate CP diagnosis,^12,13 the increasing complexity of evaluating for CP etiologies and mimics (table 1), and noting that the training backgrounds of CNs/NDDs make them poised to be effective CP diagnosticians.^31,32

It will be essential to obtain agreement from the CN/NDD community at large regarding their role as CP diagnosticians. Surveying a larger group of CNs/NDDs regarding this role can be the first step toward gauging this. Given that CP diagnostic practices and CN/NDD roles may differ between countries, an international survey pool would be additionally valuable.

If CNs/NDDs are to formally assume the role of CP diagnostician, it will be critical to ensure that training programs continue to prepare CNs/NDDs for CP diagnosis (including techniques for early diagnosis) and determination of CP etiology. To ensure that this is occurring, the adequacy of CN/NDD training in CP care should be confirmed and any discovered training gaps should be addressed. This should include inquiry regarding training in 1) health and disease of the maternal/placental/fetal triad,^36,37 2) neonatal disorders,^36,37 and 3) neurobehavioral assessment for disorders including attention deficit/hyperactivity disorder (ADHD) and autism spectrum disorder (ASD), which are common coexisting concerns in children with CP.³⁸ An additional point of focus, based on CN/NDD self-reported lack of expertise, could be on the use of infant standardized motor assessment scales as part of a rigorous approach to early CP diagnosis in high-risk infants.¹² Establishing widely accessible CP education and training resources are also essential to this mission.

Noting that perinatal risks can be identified before the manifestation of CP symptoms (table 2), there are potential benefits of CN/NDD involvement at the time these risks are first identified. In the case of significant prenatal risk factors (e.g., brain malformations^39,40 or severe intrauterine growth restriction^41,42), involvement of CNs/NDDs as fetal consultants could be helpful for family counseling and tracking of fetal neurodevelopment. In the neonatal period, involvement of CNs/NDDs can allow for optimal reconciliation between the clinical history, placental pathology, neuroimaging findings, and the neurologic examination to generate a comprehensive risk assessment for CP and initiate appropriate etiologic investigations (including genetic testing). Neonatal CN/NDD involvement could also facilitate the early identification of neurologic features consistent with known CP syndromes or CP mimics (table 1). Early and ongoing CN/NDD involvement could potentially result in earlier CP diagnosis. Eventually, fetal or neonatal consultation of CNs/NDDs could help guide initiation of neuroprotective interventions that may mitigate the risk of CP altogether. Early CN/NDD involvement could also be beneficial with regard to anticipation and management of neurodevelopmental disorders like ADHD and ASD, which cosegregate with CP but can also arise independently following similar perinatal risk factors.^43,44

Aside from the clear value of CNs/NDDs in CP diagnosis, there is a wide range of views within the CNS CP-SIG as to what extent CNs/NDDs should be involved in management of patients with CP. This requires further clarification, though CNs/NDDs felt capable of guiding comprehensive management of these patients and may be uniquely qualified to manage epilepsy in CP. The ambiguity regarding the role of CNs/NDDs in CP management could suggest a relative lack of focus in CN/NDD training on the ongoing care of children with CP after the diagnosis has been made.

The care of people with cerebral palsy is inherently multidisciplinary in nature. Comprehensive, coordinated approaches are needed to achieve optimal outcomes with each discipline bringing their unique skill sets to address the many challenges people with CP face. We hope that this marks the starting point of a multidisciplinary effort regarding how different specialties can capitalize on their unique expertise to form ideal CP care teams.

Glossary

ACGME

American College of Graduate Medical Education

CNs/NDDs

child neurologists and neurodevelopmentalists

CP

cerebral palsy

CNS

Child Neurology Society

CP-SIG

Cerebral Palsy Special Interest Group

Appendix. Authors

Study funding

Funding supporting this work is from the National Institute of Neurological Disorders and Stroke (5K12NS098482-02 and 1R01NS106298).

Disclosures

Dr. Aravamuthan receives research funding from the National Institute of Neurological Disorders and Stroke. Dr. Shevell is on the editorial boards of Pediatric Neurology and Journal of Child Neurology and receives research support from the Kids Brain Health Network and the Harvey Guyda Chair Fund of the Montreal Children's Hospital Foundation. Dr. Wilson, Dr. Kim, and Dr. O'Malley have no relevant disclosures or financial support. Dr. Pearson receives research funding from the National Institute of Neurological Disorders and Stroke. Dr. Kruer is on the editorial board of the Journal of Child Neurology and has received consulting fees from PTC Pharmaceuticals and research support from the National Institute of Neurological Disorders and Stroke and from Medtronic. Dr. Waugh receives research support from the American Academy of Neurology and the Collaborative Center for X-linked Dystonia Parkinsonism. Dr. Russman is on the Scientific Advisory Board for Sarepta: DMC. Dr. Shapiro has no relevant disclosures or financial support. Dr Tilton serves on the board of directors of the American Academy of Neurology, on the editorial boards of the Journal of Child Neurology and Neurology, and as a consultant for Ipsen Biopharmaceuticals, Inc. Dr Tilton has received personal compensation for speaking engagements and research/grant support from Ipsen Biopharmaceuticals, Inc, and receives patent royalties through her institution for botulinum toxin in the prevention and treatment of acne. Go to Neurology.org/N for full disclosures.