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Clinical Approach to a Child with Movement Disorders
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Clinical Approach to a Child with Disordered Movements Jennifer A. O′Malley, Donald L. Gilbert
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To appear in: Seminars in Pediatric Neurology Cite this article as: Jennifer A. O′Malley and Donald L. Gilbert, Clinical Approach to a Child with Disordered Movements, Seminars in Pediatric Neurology,doi:10.1016/j.spen.2017.12.001 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Seminars in Pediatric Neurology: Clinical Approach to a Child with Disordered Movements
Jennifer A. O’Malley, M.D., Ph.D.1 and Donald L. Gilbert, M.D., M.S.2 1)
Clinical Assistant Professor, Division of Child Neurology, Department of Neurology,
Stanford University, Palo Alto, California;
2)
Professor of Pediatrics and Neurology, Divi-
sion of Neurology, Department of Pediatrics, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio
Contact: Jennifer A. O’Malley MD, PhD Clinical Assistant Professor Division of Child Neurology, Department of Neurology Stanford University 730 Welch Rd Ste 206 Palo Alto, CA 94304 (650) 497-8953 (office) (650) 497-8101 (fax) [email protected]
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ABSTRACT Assessing movement can be especially challenging in children. Refined yet flexible observational exam skills and utilization of established phenomenological approaches are essential in distinguishing normal from abnormal movements in the developing child and reaching an appropriate diagnosis. Mastering such skill requires an appreciation of the unique features of the developing motor system and an understanding of key concepts underlying normal motor development in children. Establishing a trusting therapeutic relationship with the patient and family, minimizing anxiety, and utilizing observation and distraction during physical exam are essential to successful diagnosis and management.
BASIC PRINCIPLES OF MOVEMENT IN CHILDREN As child neurologists, we often first learn to assess movement in adult patients from our adult neurology mentors. Our adult neurology colleagues demonstrate and instill a well-established, organized, and methodical approach to history taking and physical exam that is efficient and effective in most cooperative adult patients. We quickly learn however, that in the pediatric setting, our approach to the neurologic exam in a child must be flexible, adaptable, and continually modified to meet the needs of our young, developing (and often not entirely cooperative) patients. The difficulty of assessing movement in a “moving target,” as the developing nervous system presents the examiner with a continuously evolving baseline, can make interpreting abnormal (and even normal) movements especially challenging in children. Mastering such skill also requires an appreciation of the unique features of the developing motor system and an
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understanding of several key concepts underlying the normal motor development process.
1) Motor control develops in an established gradient In the neonate, motor control develops in parallel with progression of central and peripheral myelination, occurring in a rostro-caudal gradient accompanied by progressively diminishing primitive reflexes and carefully timed emergence of postural reflexes [1, 2]. (Figure 1) Control of voluntary movement begins early in infancy first at the level of the head and neck, followed sequentially by upper trunk and extremity control, then lower trunk and finally leg control. With developing head control and maintaining new upright positions such as sitting, postural reflexes (such as lateral propping) emerge. It follows that such postural reflexes provide protection against head injury in the increasingly upright, rapidly developing infant. For example, as babies learn to stand, the primitive plantar grasp reflex diminishes, enabling flattening of feet and independent support of one’s weight on both legs, while additional new postural reflexes to minimize injury in event of a fall (parachuting reflex) emerge. This well-established pattern of rostro-caudal motor development accompanied by evolving postural reflexes is critical to protect one’s rapidly growing and developing complex human brain: learning to walk upright poses significant risk of future brain injury if the walker is unable to first hold his head up with good trunk control and enough upper extremity coordination to catch himself when falling.
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Failure to develop appropriate postural reflexes, or inappropriate retention of primitive reflexes are early indications of abnormal motor development.
2) Voluntary movement involves complex signaling throughout the CNS A rudimentary model of the human motor system may be limited to corticospinal tract signaling leading to muscle activation and suppression. A more refined approach is often basal ganglia centric, in recognition of the delicate balance of excitatory and inhibitory signaling that contribute to the finely tuned motor control critical to human movement [3-8]. The devoted student of neurology appreciates that human movement involves intricate and elegant coordination of numerous pathways converging to integrate complex signaling from throughout the nervous system, including not only the deep gray, motor cortex and spinal cord, but also the brainstem, cerebellum, frontal cortex, and limbic system, ultimately converging in the basal ganglia and thalamus prior to eventual corticospinal output. Our current model of human movement continues to evolve as we have an increasing understanding of the role of not only dedicated motor circuitry but also the importance of “non-motor” pathways integrating signaling from multiple levels of the central nervous system (CNS) and influencing the planning, initiation, and execution of movement.
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Conceptualizing motor control as a whole brain activity and recognizing the importance of the interplay between both traditionally motor and “non-motor” pathways involving a wide array of CNS structures provides a much richer understanding of both normal movement and movement disorders [9, 10].
3) Voluntary movement is multi-phasic Voluntary movement is not merely the execution of movement. Instead, voluntary movement is the end result of a multi-phasic sequence involving unique and overlapping signaling pathways dedicated to the planning, initiation, and execution of complex movement (as reviewed by [4, 7, 11-13]). Each phase of voluntary movement relies on signaling networks involving cortical, subcortical and cerebellar structures [14-17]. Motor planning (including learning, selection, timing and initiation of movement) involves many brain areas, primarily including cortical association areas, the basal ganglia, cerebellum and thalamus. Motor initiation is dependent upon signaling from at least the thalamus and motor cortex. Movement execution is the result of integrated signaling between motor cortex, cerebellum, brainstem, spinal cord and muscles [15, 18, 19]. Of note, there are multiple feedback loops between anatomic areas and across motor phases, the details of which are beyond the scope of this review. (Figure 2) Disordered movement may result from impairment of motor planning, initiation of movement, execution of movement, or simultaneous impairment of multiple motor phases localizing to one or several anatomic areas [7]. Understanding and conceptualizing voluntary movement as a multi-phasic process is extremely helpful when trying to characterize, anatomically localize, and treat abnormal movements in patients.
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4) Motor control requires a balance of inhibitory and excitatory signaling While the specific pathways involved in voluntary movement are complex, it can be helpful to conceptualize motor control as a finely tuned balance of “gas and brakes,” as the basal ganglia serve as the center of dopaminergic modulation of excitatory glutamatergic (the “gas”) and inhibitory GABAergic (the “brakes”) signaling [20]. To briefly review, there are 3 major pathways of signaling through the basal ganglia; the direct, hyperdirect, and indirect pathways [21-24]. The direct pathway ultimately increases cortical excitation, through relieving pallidal inhibition of thalamocortical output, hence facilitating (and selecting) movement. In contrast, both the hyperdirect and indirect pathways ultimately decrease cortical excitation, through enhanced pallidal inhibition of thalamocortical output, hence suppressing and regulating movement. Dopamine functions as a modulator in this balance of inhibitory and excitatory signaling, ultimately allowing for selection of desired movements and inhibition of opposing or unwanted movements [6, 11, 15, 16, 25-27]. The complex signaling leading to selective motor excitation and inhibition, and the influence of additional brain areas on basal ganglia mediated integration of motor signaling are areas of continued discovery [28-33].
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5) Extra movements in children are not always abnormal; teaching the neurology learner about pediatric movement disorders In developing children, it can be difficult to distinguish between typical and pathologic movement. This is an especially important point when teaching the movement exam to neurology learners such as medical students and residents. In neurology, and especially in pediatric movement disorders, a live or video exam demonstrating the movement in question is invaluable. Diagnosis of movement disorders requires direct observation in order to describe phenomenology. Not only is a live exam or video effective in teaching basic principles of assessing movement in children, it is also an interactive and fun method for both experienced and new neurology learners. Videos of normal children at various developmental stages provide a fun and energizing learning opportunity for learners. We keep a running list of links to our favorite publicly available videos demonstrating typical motor development in children of various ages. We then present these videos to students with no background information and a chief complaint of “funny movements.” We challenge the learner to describe what she sees and to hone observation skills to deliver as complete of a neurologic exam as possible. The learner is not told if the exam is normal or abnormal. For example, careful observation of a typically developing but newly walking toddler may elicit an array of detailed descriptions suspicious of ataxia, dysmetria, tremor, and titubation from a new neurology learner. The exercise of breaking down normal movements and finding accurate descriptive terms begins to build a foundation of movement vocabulary and observation skills that are essential to later description and diagnosis of pathologic movement phenomenology.
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These foundational principles of the developing motor system help us understand when movement goes awry and provide a starting point from which to evaluate the child who presents with concern for abnormal movement.
THE OFFICE VISIT Taking a movement history A reliable movement disorders evaluation of course begins with an effective and accurate movement history. The goal of the history is to be simultaneously comprehensive, accurate and efficient. Additionally, the provider is working to establish a trusting and therapeutic relationship with both the child and the child’s caregivers. It is ideal to conduct as much of the interview and history taking directly with the child as possible. Observing a child’s ability to describe the movement(s) of concern often answers many key questions as outlined below. Also, observing the caregiver’s ability to allow the child to provide history can be very telling of family dynamics that may influence your approach and formulation of a care plan. When the child is nonverbal or too young to provide history, direct interaction with the child throughout the interview with the guardian is still important as it provides an excellent opportunity to observe the child’s baseline movements. Assessing movement relies on a phenomenological, or pattern recognition, based approach focused on identification of key components such as timing, localization, and characteristic features of the movements in question.
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A comprehensive movement history provides the following information: Describing and defining the phenomenology of the abnormal movement: Is the child aware of the movement in question or episodes? Who notices or is bothered most by the movements? Often the parent or teacher is aware of and bothered by the movement, but the child may be unaware. Does the child experience the movements as voluntary (“I am doing it”), involuntary (“it just happens”) or both? Identify any provoking/exacerbating/relieving/associated factors. Are the movements better/worse at certain times of day? Are the movements present or absent with sleep? Are the movements associated with any premonitory sensations or urges? Do they bring about relief? Are they suppressible voluntarily or with sensory tricks? Are the movements associated with any other neurologic or non-neurologic signs or symptoms? Try to determine the impact of the undesired movements on the child. Do they cause pain? Do they interfere with function? Are they socially embarrassing? Has the child undergone any prior evaluations, seen any other physicians for this complaint, or undergone any prior testing/work-up?
Birth history: Birth history should include infant’s birth weight and head circumference, gestational age, known complications during pregnancy and/or delivery; any prolonged nursery or NICU stay (did infant come home with parent from hospital or did either baby or mother have prolonged stay and if so for what?), any history of jaundice requiring phototherapy and/or transfusion and history of in utero maternal substance abuse.
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Developmental history: A clear and detailed developmental history is critical in assessing abnormal movement in children. It is of particular importance to ask about any motor delay that has “caught up,” and look for evidence of compensatory behaviors from the child, which may mask a subtle fine or gross motor delay.
Determining associated psychologic factors: It is helpful to determine if the abnormal movements are associated with anxiety, depression, obsessive compulsive disorder (OCD), attention deficit hyperactivity disorder (ADHD) or other psychologic factors. The parents or medical records may indicate prior formal developmental or psychiatric diagnoses. Discussing psychological factors accompanying movement disorders can be challenging and must be done in a manner sensitive to both the child and his guardians. Families are often more comfortable discussing their child’s “worries” compared to using the label of “anxiety.” It can be helpful to first normalize anxiety by simply saying “As people, we all have worries and some of us worry more than others.” Then to the child: “Do you think you are “an expert worrier?” Or to the parents: “Is your child an ‘expert worrier’ or does your child seems to worry more than other children his age?” Asking about anxiety first can open the doors to further discussion of other mood disorders. It is important to ask if the child has ever struggled with extended periods of sadness, or if the parents have ever worried their child could be depressed. Obsessivecompulsive disorder and traits are common in many pediatric movement disorders. Asking sensitively whether the child has “habits” or if the child “becomes very upset when
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his schedule is interrupted, or if the day doesn’t go according to planned” can be revealing of obsessive thoughts or compulsive behaviors. In screening for ADHD, ask about inattention, hyperactivity, and impulsivity. It can be helpful to ask questions such as “When you get in trouble at school is it for getting out of your seat without asking? …having trouble keeping your hands to yourself? …talking out of turn or blurting out in class?”
Evaluating the impact of the abnormal movement in the child’s life: Asking about psychological factors naturally leads to discussion about school performance and screening for teasing, bullying by peers at school, or inappropriate responses to the movements by school staff. It is important to ask the parent and child about this, as their perspectives may differ [34]. Are the movements disruptive to learning, to the classroom, or at home? Are these movements preventing the child from going to social events or preventing the family from taking the child out in public? How is the child’s school performance? Has he had prior academic testing and if so, what were the results? Does the child have any formal educational accommodations or extra assistance in place?
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Family history: It is ideal to build a three-generation genogram including any family history of similar movements, movement disorders as a child, or other neurologic disease. Encourage the parents to ask their extended family if they themselves had history of any transient abnormal movements or habits as children they may not have known about or recognized. The recollections of grandparents, aunts, and uncles can be very revealing. Other important points of family history include tactful screening for consanguinity as well as sensitively inquiring for history of pregnancy loss or early infant death.
Social history: A thorough social history is incredibly important given the strong influence of psycho-social factors in movement disorders. The following questions can provide valuable social history information: Who does the child live with? Has the living situation changed recently? Have there been any changes on where the child lives, who the child lives with, who is living in the home? Any new jobs for caregivers? Any new schools/teachers/classrooms/daycare/nanny etc for the child?
Other medical history: In addition to typical review of medical and surgical histories it is important to obtain a sleep and diet history. In particular, the diet history should be inclusive of any dietary and/or medical supplements with specific questioning about cannabis and/or hemp product use in cases of children with spasticity, dystonia, and epilepsy. These products
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are now widely and readily available via internet purchase, though many families are hesitant to disclose use unless asked directly. Finally, with even the most careful history, it can be easy for both parents and clinicians to misinterpret a child’s symptoms. Thus careful re-evaluation and detailed physical exam are critical for accurate diagnosis. Consider for example, the case of a 7 year old girl who presented to neurology clinic with new urinary incontinence and no other complaints. Detailed history revealed the true etiology of her apparent incontinence was actually new clumsiness preventing efficient and independent clothing removal necessary to use the toilet quickly enough to avoid urinary accidents. This history, coupled with acute distal hand weakness and sensory deficit on exam, redirected the visit to the correct diagnosis of acute inflammatory demyelinating polyneuropathy (AIDP) followed by appropriate management.
The pediatric movement disorder exam Exam approach: The pediatric movement exam is highly dependent on careful observation. Distraction is an essential technique, helpful to nearly all pediatric exams, and is especially useful when attempting to observe complex movements and/or behaviors. However, in movement disorders, where many diagnoses are accompanied by psychiatric symptoms such as anxiety, it can be quite difficult for children to be relaxed and unbothered by the examiner in the exam room. It is immensely valuable to observe the child without the child’s knowledge. This can be accomplished using observation through a peep hole
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in the exam room door, or while the child is distracted and playing with a sibling during the appointment. Sometimes the diagnosis may be clear just by watching the child walk from the waiting room to the exam room. The amount of information one can obtain from simple observation is greatly increased when a child is relaxed and distracted. Thus, developing a relaxed (but thorough), child-focused approach that minimizes anxiety for both the patient and family will maximize information obtained during a visit. A flexible and creative approach is essential in obtaining a full neurologic exam from an apprehensive or uncooperative child. The simple act of integrating toys (especially those that light up or are interactive) can help a nervous and frightened child become relaxed and engaged. More complex activities such as reading a book with a child in the exam room can demonstrate multiple neurologic exam findings such as cognitive/speech ability, attention, eye movements (saccades, accommodation), tone, gross motor (ability to sit, head control), fine motor control (pointing, turning pages, manipulating small objects, holding book, transfer), cerebellar function (eye movements, head/limb tremor), etc. Other times, simply bringing the child and family out of the exam room and into the hallway, or even outside if possible can significantly reduce a child’s anxiety and allow for much better observation of the child’s exam. When it is not possible to directly observe the child in a relaxed and distracted state, parental home videos of the child at home, in school, etc. can serve as a helpful adjunct to in-person observation. Sending parents home with explicit written instructions of what activities you would like them to video can provide key information.
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General exam: On general exam it is important to note any facial dysmorphism that may suggest an identifiable syndrome. Identify abnormalities in vision, eye appearance, alignment, or movement. Gross assessment of hearing should be performed. Note any unique skin findings that could be suggestive of an underlying neurocutaneous syndrome. Basic heart/lung and thyroid exams are important in ruling out extra-cranial causes of dyskinetic movements. Abdominal exam will help rule out organomegaly to reassure against storage disease. Musculoskeletal evaluation should note abnormalities in the structure of the trunk or limbs.
Neurologic exam: On neurologic exam for abnormal movements, a careful eye examination is of utmost importance. Look for tics, nystagmus, abnormal extra-ocular movements, saccades and evidence of oculomotor apraxia or opsoclonus. Cranial nerve examination allows for thorough evaluation of brainstem and cerebellar function. Abnormal speech patterns may suggest brainstem or cerebellar dysfunction or could also reflect accompanying behavioral/developmental delay and/or anxiety.
Tone: Careful assessment of tone in multiple phases of activation is the initial step to a thorough motor exam in a child with disordered movements. Ideally, the child is observed at both rest and during activity. Tone can be particularly difficult to assess, especially in the child who has spasticity, dystonia, or dyskinesias. The initial approach in-
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volves a determination of whether the child has normal tone while fully at rest and whether that tone abnormality involves the extremities alone or in combination with the head/trunk. A child who appears stiff with high tone may actually have hypotonia with overlying spasticity, or relatively normal baseline tone with action-induced dystonia, or just be nervous and unable to relax. Usually, children with isolated dystonia do not have rigidity, cogwheeling, or elevated tone at rest and so these findings should be identified if present. Spasticity, with tone that increases with velocity, demonstrates spastic catch, and has resulted in contractures is more common. The distinction is important to narrowing a differential diagnosis, but often in hypertonic children there is a mixture of spasticity and dystonia.
Bulk: Assessment of bulk includes evaluating for atrophy and asymmetry. In contrast, increased bulk or muscle definition, which is atypical in young children, can be a sign of chronic muscle overactivity. This can be seen in children with dystonia due to excessive patterns of activation during routine movement. It also can indicate low subcutaneous fat stores secondary to chronic over-activity.
Strength: When manual muscle testing is not feasible due to the age of a child, strength can be assessed by monitoring the child during play. Can the child sit independently, holding his head steady? Can he stand and walk without assistance? Can he climb into his parent’s lap, run, jump, or lift toys above his head?
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Is the child quick to perform actions or does he need extra time to initiate movements? Does he perform movements efficiently using only the involved extremities or does he have excess movements in neighboring or contralateral muscle groups that interfere with execution of a desired task? Does he perform movements slowly or irregularly?
Sensory: Of note, the sensory exam can be unreliable in children. Minor discrepancies are commonly reported by children or adolescents with intact sensation and often times a detailed sensory exam is relatively low-yield in a child. In anxious children, the sensory exam can be particularly difficult and may contribute to worsened anxiety or new complaints. Thus, abnormalities on exam should be interpreted cautiously, and confirmed with repeat examination.
Cerebellum: Cerebellar examination is ongoing throughout the exam and includes eye movements, speech articulation and pacing, postural control, limb control, and gait. Additional evaluation for tremor is an important component of the movement exam. Coordination assessment and interpretation of findings are highly age dependent. In infants, observation of feeding can be very helpful. In older children use of small stacking blocks is helpful in demonstrating hand use and hand-eye coordination.
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Motor exam techniques for specific diagnoses: Distraction, play, and other similar techniques are especially helpful in enhancing and/or minimizing movements in question. For example, dystonia, chorea, tremor, and other movements may intensify when the patient is demonstrating the movement with intention, but can improve when the child is performing other tasks that utilize the same muscles, but is distracted from the problem by a toy or other engaging activity. In children with tics, it can be helpful during the exam to ask a child to demonstrate (and then suppress) his or her motor and/or vocal tics. Frequent tics can generally be shown to diminish or stop during purposeful movements of the same muscle groups. For children with suspected chorea, observe the child for restlessness while sitting quietly and check for exacerbation during actions. Also check for motor impersistence, the inability to sustain voluntary action, by having the child grip the examiner’s two fingers with their two hands simultaneously (where the impersistence and regripping is termed “milkmaid’s grip”) and protrude the tongue (where the impersistence causes the protruding tongue to dart in and out). In evaluation of dystonia look for unusual patterns of muscle co-contractions that cause jerking and posturing in a dynamic fashion, influenced differentially depending on the type of action including reaching, maintaining limbs extended in various postures, and walking. Be sure to check for subtle sensory tricks, also called gestes antagonistes. Attempt to provoke episodic dystonia in the office. When doing so, be careful to discern whether the patient has action-induced dystonia versus less commonly, paroxysmal ki-
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nesigenic dystonia. Watch carefully for evidence of involvement in other limbs or muscles beyond those reported by the patient. Evaluation of tremor should determine whether the tremor occurs at rest, which is a red flag for a hypokinetic rigid disease in children, versus with action; in particular, maintaining limbs outstretched for postural tremor and reaching repeatedly to a target for intention tremor. Document the anatomic distribution of the tremor and whether the tremor has a regular or irregular, jerky oscillation that varies with position. Use of an Archimedes spiral worksheet can help to quantify tremor. Activities such as pouring water into a cup and holding cup of water outstretched are also helpful in detecting tremor. Watch closely for tremor variability with distraction, hand position, or specific motor tasking as this can be especially helpful when narrowing your differential. Parkinsonism is rare in children but should not be missed. If rigidity or cogwheeling was noted on tone exam, it is helpful to videotape the hands at rest and to pay careful attention to facial expressiveness, and fluid initiation of movement and movement speed. Current and prior medication and/or drug exposure should always be considered when determining etiology of parkinsonism in a child. Psychogenic movements are very common in children and often (but not always) improve with distraction on exam. Psychogenic tremor, tics, and chorea may be entrainable. Nevertheless, it is equally important to note that anxiety is very common with organic movement problems and may contribute to waxing/waning symptoms making it more difficult to clearly identify an organic movement disorder. Regardless of etiology, many abnormal movements will worsen as anxiety heightens and conversely also improve with improvement in anxiety. Thus, it is prudent to be cautious when attributing a
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movement to psychogenic causes, particularly when the phenomenology is dystonic. Children often subconsciously embellish or disguise abnormal movements. This again highlights the importance of observation in multiple environments and emotional states to achieve and accurate diagnosis. Movement disorders in children are often mixed. For example, a child with chorea may also demonstrate accompanying dystonia. In these cases, it is helpful to first identify the movement that is most interfering with function. This approach will then further guide decision making for treatment and intervention. Movement rating scales can also be helpful and appropriate tools for evaluation and monitoring of symptoms in specific diseases.
Testing and observing parents and siblings during patient visit It is important to carefully observe parents and siblings when considering possible etiologies of abnormal movements in children. Essential tremor can be more easily diagnosed by performing a tremor exam for both parents and siblings. Parents may have an unrecognized history of prior and even current tics, dismissed in their own childhood as ‘habits.’ Mild dystonia may also go unrecognized or dismissed. If a child presents with writer’s cramp, observing handwriting samples from not only the child but also his parents can be essential to the diagnosis of an underlying primary dystonia.
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Multimedia exam: Accurate diagnosis from phenomenology is greatly aided by video exam when available [20, 35-37]. Further group review of video exam with colleagues with experience in movement disorders can be especially helpful in obtaining an accurate diagnosis. One unique advantage is the video exam serves to accurately capture a child’s exam at specific time intervals. Movement disorders that are particularly difficult to diagnose in real time can be captured on video and slowed down for careful assessment. Additionally, asking the parents for photos and old home videos can be particularly helpful in assessing episodic movements that are unobservable in the clinic or in the case of progressive decline in motor exam over time.
REACHING A DIAGNOSIS Refining a differential diagnosis for disordered movement in children: Movement specialists typically rely on a phenomenological approach to characterization of movement disorders in both adults and children [38-41]. Consideration of the complex motor circuitry involved in both normal and abnormal movements supports first using phenomenology (rather than anatomy) to classify and subdivide pediatric and adult movement disorders. A phenomenological approach relies on skilled pattern recognition on history and exam in order to identify the most likely diagnosis and helps distinguish between ataxia, athetosis, ballism, chorea, dystonia, myoclonus, parkinsonism, stereotypies, tics, and tremor. The most common pediatric movement disorders such as tics, stereotypies, developmental tremor, and abnormal movements associated
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with underlying static encephalopathy are typically quickly identifiable using a phenomenological approach. Often the phenomenology, when coupled with information from your detailed history in addition to the age and developmental state of the child, can quickly lead to a clear diagnosis, or will at least guide potential localization of the abnormal movements to a specific anatomic site. Additional anatomic localization may be dependent upon neuroimaging such as brain magnetic resonance imaging (MRI). The differential diagnosis can often be further narrowed once the history, time course, and age of patient at symptom onset are taken into consideration. It is important to remember the caveat that some movement disorders present differently in children compared to adults. Such detailed characterization of disease phenotype may assist in further determination of associated genotype, or at least aid in narrowing choices for initial genetic testing. In cases where phenomenology and history are not enough to make a clear diagnosis it is always important to rule out secondary causes considering etiologies such as drug/toxin use/exposure/ingestion/withdrawal, movements due to other neurologic diagnoses such as migraine or seizures, infection, inflammatory processes, vascular and traumatic etiologies, metabolic or mitochondrial disease, and other genetic conditions. For more complex diagnoses, experts in the field advocate for a stepwise, methodical assessment of phenomenology [20, 36] to further assess complex movement. We have outlined a phenomenological approach, as modified from previously published approaches [20, 39]. (Figure 3) Reviewing formal definitions of movement disorders can also be helpful [42-44].
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In the following articles of this special movement disorders edition of Seminars in Pediatric Neurology authors will guide you through differential diagnosis and details about a number of important diagnoses and pathologies in pediatric movement disorders ranging from very common childhood habits, stereotypes and tics, to much rarer neurologic conditions. Additional components of history taking and physical exam techniques and findings will be addressed according to the specific phenomenology discussed in each chapter.
Disclosure of interests: Dr. Gilbert has received honoraria and/or travel support from the Tourette Syndrome Association, the American Academy of Pediatrics, and the Child Neurology Society. He has received book royalties from Elsevier and Wolters Kluwer. He has received compensation for expert testimony for the U.S. D.O.J. D.V.I.C. program. Dr. Gilbert has received research support from the NIH (NIMH, NINDS). He has received funding for work as a clinical trial site investigator from Ecopipam Pharmaceuticals (clinical trial, Tourette Syndrome) and EryDel (clinical trial, Ataxia Telangiectasia).
The authors have no commercial, proprietary, or financial interest in any products or companies described in this article.
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Figure 1: Motor control develops in parallel with central and peripheral myelination, occurring in a rostro-caudal gradient accompanied by progressively diminishing primitive reflexes and carefully timed emergence of postural reflexes.
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Figure 2: A schematic representation of the major anatomical brain areas and functional pathways involved in each phase of voluntary movement. There are extensive feedback loops and overlap of signaling, as suggested by the high degree of overlap between brain areas designated in the figure.
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Figure 3: Schematic representation of the diagnostic approach to children with movement disorders.
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image
Clinical Approach to a Child with Disordered Movements Jennifer A. O′Malley, Donald L. Gilbert
www.elsevier.com/locate/bios
PII: DOI: Reference:
S1071-9091(17)30150-X https://doi.org/10.1016/j.spen.2017.12.001 YSPEN695
To appear in: Seminars in Pediatric Neurology Cite this article as: Jennifer A. O′Malley and Donald L. Gilbert, Clinical Approach to a Child with Disordered Movements, Seminars in Pediatric Neurology,doi:10.1016/j.spen.2017.12.001 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Seminars in Pediatric Neurology: Clinical Approach to a Child with Disordered Movements
Jennifer A. O’Malley, M.D., Ph.D.1 and Donald L. Gilbert, M.D., M.S.2 1)
Clinical Assistant Professor, Division of Child Neurology, Department of Neurology,
Stanford University, Palo Alto, California;
2)
Professor of Pediatrics and Neurology, Divi-
sion of Neurology, Department of Pediatrics, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio
Contact: Jennifer A. O’Malley MD, PhD Clinical Assistant Professor Division of Child Neurology, Department of Neurology Stanford University 730 Welch Rd Ste 206 Palo Alto, CA 94304 (650) 497-8953 (office) (650) 497-8101 (fax) [email protected]
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ABSTRACT Assessing movement can be especially challenging in children. Refined yet flexible observational exam skills and utilization of established phenomenological approaches are essential in distinguishing normal from abnormal movements in the developing child and reaching an appropriate diagnosis. Mastering such skill requires an appreciation of the unique features of the developing motor system and an understanding of key concepts underlying normal motor development in children. Establishing a trusting therapeutic relationship with the patient and family, minimizing anxiety, and utilizing observation and distraction during physical exam are essential to successful diagnosis and management.
BASIC PRINCIPLES OF MOVEMENT IN CHILDREN As child neurologists, we often first learn to assess movement in adult patients from our adult neurology mentors. Our adult neurology colleagues demonstrate and instill a well-established, organized, and methodical approach to history taking and physical exam that is efficient and effective in most cooperative adult patients. We quickly learn however, that in the pediatric setting, our approach to the neurologic exam in a child must be flexible, adaptable, and continually modified to meet the needs of our young, developing (and often not entirely cooperative) patients. The difficulty of assessing movement in a “moving target,” as the developing nervous system presents the examiner with a continuously evolving baseline, can make interpreting abnormal (and even normal) movements especially challenging in children. Mastering such skill also requires an appreciation of the unique features of the developing motor system and an
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understanding of several key concepts underlying the normal motor development process.
1) Motor control develops in an established gradient In the neonate, motor control develops in parallel with progression of central and peripheral myelination, occurring in a rostro-caudal gradient accompanied by progressively diminishing primitive reflexes and carefully timed emergence of postural reflexes [1, 2]. (Figure 1) Control of voluntary movement begins early in infancy first at the level of the head and neck, followed sequentially by upper trunk and extremity control, then lower trunk and finally leg control. With developing head control and maintaining new upright positions such as sitting, postural reflexes (such as lateral propping) emerge. It follows that such postural reflexes provide protection against head injury in the increasingly upright, rapidly developing infant. For example, as babies learn to stand, the primitive plantar grasp reflex diminishes, enabling flattening of feet and independent support of one’s weight on both legs, while additional new postural reflexes to minimize injury in event of a fall (parachuting reflex) emerge. This well-established pattern of rostro-caudal motor development accompanied by evolving postural reflexes is critical to protect one’s rapidly growing and developing complex human brain: learning to walk upright poses significant risk of future brain injury if the walker is unable to first hold his head up with good trunk control and enough upper extremity coordination to catch himself when falling.
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Failure to develop appropriate postural reflexes, or inappropriate retention of primitive reflexes are early indications of abnormal motor development.
2) Voluntary movement involves complex signaling throughout the CNS A rudimentary model of the human motor system may be limited to corticospinal tract signaling leading to muscle activation and suppression. A more refined approach is often basal ganglia centric, in recognition of the delicate balance of excitatory and inhibitory signaling that contribute to the finely tuned motor control critical to human movement [3-8]. The devoted student of neurology appreciates that human movement involves intricate and elegant coordination of numerous pathways converging to integrate complex signaling from throughout the nervous system, including not only the deep gray, motor cortex and spinal cord, but also the brainstem, cerebellum, frontal cortex, and limbic system, ultimately converging in the basal ganglia and thalamus prior to eventual corticospinal output. Our current model of human movement continues to evolve as we have an increasing understanding of the role of not only dedicated motor circuitry but also the importance of “non-motor” pathways integrating signaling from multiple levels of the central nervous system (CNS) and influencing the planning, initiation, and execution of movement.
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Conceptualizing motor control as a whole brain activity and recognizing the importance of the interplay between both traditionally motor and “non-motor” pathways involving a wide array of CNS structures provides a much richer understanding of both normal movement and movement disorders [9, 10].
3) Voluntary movement is multi-phasic Voluntary movement is not merely the execution of movement. Instead, voluntary movement is the end result of a multi-phasic sequence involving unique and overlapping signaling pathways dedicated to the planning, initiation, and execution of complex movement (as reviewed by [4, 7, 11-13]). Each phase of voluntary movement relies on signaling networks involving cortical, subcortical and cerebellar structures [14-17]. Motor planning (including learning, selection, timing and initiation of movement) involves many brain areas, primarily including cortical association areas, the basal ganglia, cerebellum and thalamus. Motor initiation is dependent upon signaling from at least the thalamus and motor cortex. Movement execution is the result of integrated signaling between motor cortex, cerebellum, brainstem, spinal cord and muscles [15, 18, 19]. Of note, there are multiple feedback loops between anatomic areas and across motor phases, the details of which are beyond the scope of this review. (Figure 2) Disordered movement may result from impairment of motor planning, initiation of movement, execution of movement, or simultaneous impairment of multiple motor phases localizing to one or several anatomic areas [7]. Understanding and conceptualizing voluntary movement as a multi-phasic process is extremely helpful when trying to characterize, anatomically localize, and treat abnormal movements in patients.
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4) Motor control requires a balance of inhibitory and excitatory signaling While the specific pathways involved in voluntary movement are complex, it can be helpful to conceptualize motor control as a finely tuned balance of “gas and brakes,” as the basal ganglia serve as the center of dopaminergic modulation of excitatory glutamatergic (the “gas”) and inhibitory GABAergic (the “brakes”) signaling [20]. To briefly review, there are 3 major pathways of signaling through the basal ganglia; the direct, hyperdirect, and indirect pathways [21-24]. The direct pathway ultimately increases cortical excitation, through relieving pallidal inhibition of thalamocortical output, hence facilitating (and selecting) movement. In contrast, both the hyperdirect and indirect pathways ultimately decrease cortical excitation, through enhanced pallidal inhibition of thalamocortical output, hence suppressing and regulating movement. Dopamine functions as a modulator in this balance of inhibitory and excitatory signaling, ultimately allowing for selection of desired movements and inhibition of opposing or unwanted movements [6, 11, 15, 16, 25-27]. The complex signaling leading to selective motor excitation and inhibition, and the influence of additional brain areas on basal ganglia mediated integration of motor signaling are areas of continued discovery [28-33].
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5) Extra movements in children are not always abnormal; teaching the neurology learner about pediatric movement disorders In developing children, it can be difficult to distinguish between typical and pathologic movement. This is an especially important point when teaching the movement exam to neurology learners such as medical students and residents. In neurology, and especially in pediatric movement disorders, a live or video exam demonstrating the movement in question is invaluable. Diagnosis of movement disorders requires direct observation in order to describe phenomenology. Not only is a live exam or video effective in teaching basic principles of assessing movement in children, it is also an interactive and fun method for both experienced and new neurology learners. Videos of normal children at various developmental stages provide a fun and energizing learning opportunity for learners. We keep a running list of links to our favorite publicly available videos demonstrating typical motor development in children of various ages. We then present these videos to students with no background information and a chief complaint of “funny movements.” We challenge the learner to describe what she sees and to hone observation skills to deliver as complete of a neurologic exam as possible. The learner is not told if the exam is normal or abnormal. For example, careful observation of a typically developing but newly walking toddler may elicit an array of detailed descriptions suspicious of ataxia, dysmetria, tremor, and titubation from a new neurology learner. The exercise of breaking down normal movements and finding accurate descriptive terms begins to build a foundation of movement vocabulary and observation skills that are essential to later description and diagnosis of pathologic movement phenomenology.
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These foundational principles of the developing motor system help us understand when movement goes awry and provide a starting point from which to evaluate the child who presents with concern for abnormal movement.
THE OFFICE VISIT Taking a movement history A reliable movement disorders evaluation of course begins with an effective and accurate movement history. The goal of the history is to be simultaneously comprehensive, accurate and efficient. Additionally, the provider is working to establish a trusting and therapeutic relationship with both the child and the child’s caregivers. It is ideal to conduct as much of the interview and history taking directly with the child as possible. Observing a child’s ability to describe the movement(s) of concern often answers many key questions as outlined below. Also, observing the caregiver’s ability to allow the child to provide history can be very telling of family dynamics that may influence your approach and formulation of a care plan. When the child is nonverbal or too young to provide history, direct interaction with the child throughout the interview with the guardian is still important as it provides an excellent opportunity to observe the child’s baseline movements. Assessing movement relies on a phenomenological, or pattern recognition, based approach focused on identification of key components such as timing, localization, and characteristic features of the movements in question.
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A comprehensive movement history provides the following information: Describing and defining the phenomenology of the abnormal movement: Is the child aware of the movement in question or episodes? Who notices or is bothered most by the movements? Often the parent or teacher is aware of and bothered by the movement, but the child may be unaware. Does the child experience the movements as voluntary (“I am doing it”), involuntary (“it just happens”) or both? Identify any provoking/exacerbating/relieving/associated factors. Are the movements better/worse at certain times of day? Are the movements present or absent with sleep? Are the movements associated with any premonitory sensations or urges? Do they bring about relief? Are they suppressible voluntarily or with sensory tricks? Are the movements associated with any other neurologic or non-neurologic signs or symptoms? Try to determine the impact of the undesired movements on the child. Do they cause pain? Do they interfere with function? Are they socially embarrassing? Has the child undergone any prior evaluations, seen any other physicians for this complaint, or undergone any prior testing/work-up?
Birth history: Birth history should include infant’s birth weight and head circumference, gestational age, known complications during pregnancy and/or delivery; any prolonged nursery or NICU stay (did infant come home with parent from hospital or did either baby or mother have prolonged stay and if so for what?), any history of jaundice requiring phototherapy and/or transfusion and history of in utero maternal substance abuse.
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Developmental history: A clear and detailed developmental history is critical in assessing abnormal movement in children. It is of particular importance to ask about any motor delay that has “caught up,” and look for evidence of compensatory behaviors from the child, which may mask a subtle fine or gross motor delay.
Determining associated psychologic factors: It is helpful to determine if the abnormal movements are associated with anxiety, depression, obsessive compulsive disorder (OCD), attention deficit hyperactivity disorder (ADHD) or other psychologic factors. The parents or medical records may indicate prior formal developmental or psychiatric diagnoses. Discussing psychological factors accompanying movement disorders can be challenging and must be done in a manner sensitive to both the child and his guardians. Families are often more comfortable discussing their child’s “worries” compared to using the label of “anxiety.” It can be helpful to first normalize anxiety by simply saying “As people, we all have worries and some of us worry more than others.” Then to the child: “Do you think you are “an expert worrier?” Or to the parents: “Is your child an ‘expert worrier’ or does your child seems to worry more than other children his age?” Asking about anxiety first can open the doors to further discussion of other mood disorders. It is important to ask if the child has ever struggled with extended periods of sadness, or if the parents have ever worried their child could be depressed. Obsessivecompulsive disorder and traits are common in many pediatric movement disorders. Asking sensitively whether the child has “habits” or if the child “becomes very upset when
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his schedule is interrupted, or if the day doesn’t go according to planned” can be revealing of obsessive thoughts or compulsive behaviors. In screening for ADHD, ask about inattention, hyperactivity, and impulsivity. It can be helpful to ask questions such as “When you get in trouble at school is it for getting out of your seat without asking? …having trouble keeping your hands to yourself? …talking out of turn or blurting out in class?”
Evaluating the impact of the abnormal movement in the child’s life: Asking about psychological factors naturally leads to discussion about school performance and screening for teasing, bullying by peers at school, or inappropriate responses to the movements by school staff. It is important to ask the parent and child about this, as their perspectives may differ [34]. Are the movements disruptive to learning, to the classroom, or at home? Are these movements preventing the child from going to social events or preventing the family from taking the child out in public? How is the child’s school performance? Has he had prior academic testing and if so, what were the results? Does the child have any formal educational accommodations or extra assistance in place?
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Family history: It is ideal to build a three-generation genogram including any family history of similar movements, movement disorders as a child, or other neurologic disease. Encourage the parents to ask their extended family if they themselves had history of any transient abnormal movements or habits as children they may not have known about or recognized. The recollections of grandparents, aunts, and uncles can be very revealing. Other important points of family history include tactful screening for consanguinity as well as sensitively inquiring for history of pregnancy loss or early infant death.
Social history: A thorough social history is incredibly important given the strong influence of psycho-social factors in movement disorders. The following questions can provide valuable social history information: Who does the child live with? Has the living situation changed recently? Have there been any changes on where the child lives, who the child lives with, who is living in the home? Any new jobs for caregivers? Any new schools/teachers/classrooms/daycare/nanny etc for the child?
Other medical history: In addition to typical review of medical and surgical histories it is important to obtain a sleep and diet history. In particular, the diet history should be inclusive of any dietary and/or medical supplements with specific questioning about cannabis and/or hemp product use in cases of children with spasticity, dystonia, and epilepsy. These products
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are now widely and readily available via internet purchase, though many families are hesitant to disclose use unless asked directly. Finally, with even the most careful history, it can be easy for both parents and clinicians to misinterpret a child’s symptoms. Thus careful re-evaluation and detailed physical exam are critical for accurate diagnosis. Consider for example, the case of a 7 year old girl who presented to neurology clinic with new urinary incontinence and no other complaints. Detailed history revealed the true etiology of her apparent incontinence was actually new clumsiness preventing efficient and independent clothing removal necessary to use the toilet quickly enough to avoid urinary accidents. This history, coupled with acute distal hand weakness and sensory deficit on exam, redirected the visit to the correct diagnosis of acute inflammatory demyelinating polyneuropathy (AIDP) followed by appropriate management.
The pediatric movement disorder exam Exam approach: The pediatric movement exam is highly dependent on careful observation. Distraction is an essential technique, helpful to nearly all pediatric exams, and is especially useful when attempting to observe complex movements and/or behaviors. However, in movement disorders, where many diagnoses are accompanied by psychiatric symptoms such as anxiety, it can be quite difficult for children to be relaxed and unbothered by the examiner in the exam room. It is immensely valuable to observe the child without the child’s knowledge. This can be accomplished using observation through a peep hole
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in the exam room door, or while the child is distracted and playing with a sibling during the appointment. Sometimes the diagnosis may be clear just by watching the child walk from the waiting room to the exam room. The amount of information one can obtain from simple observation is greatly increased when a child is relaxed and distracted. Thus, developing a relaxed (but thorough), child-focused approach that minimizes anxiety for both the patient and family will maximize information obtained during a visit. A flexible and creative approach is essential in obtaining a full neurologic exam from an apprehensive or uncooperative child. The simple act of integrating toys (especially those that light up or are interactive) can help a nervous and frightened child become relaxed and engaged. More complex activities such as reading a book with a child in the exam room can demonstrate multiple neurologic exam findings such as cognitive/speech ability, attention, eye movements (saccades, accommodation), tone, gross motor (ability to sit, head control), fine motor control (pointing, turning pages, manipulating small objects, holding book, transfer), cerebellar function (eye movements, head/limb tremor), etc. Other times, simply bringing the child and family out of the exam room and into the hallway, or even outside if possible can significantly reduce a child’s anxiety and allow for much better observation of the child’s exam. When it is not possible to directly observe the child in a relaxed and distracted state, parental home videos of the child at home, in school, etc. can serve as a helpful adjunct to in-person observation. Sending parents home with explicit written instructions of what activities you would like them to video can provide key information.
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General exam: On general exam it is important to note any facial dysmorphism that may suggest an identifiable syndrome. Identify abnormalities in vision, eye appearance, alignment, or movement. Gross assessment of hearing should be performed. Note any unique skin findings that could be suggestive of an underlying neurocutaneous syndrome. Basic heart/lung and thyroid exams are important in ruling out extra-cranial causes of dyskinetic movements. Abdominal exam will help rule out organomegaly to reassure against storage disease. Musculoskeletal evaluation should note abnormalities in the structure of the trunk or limbs.
Neurologic exam: On neurologic exam for abnormal movements, a careful eye examination is of utmost importance. Look for tics, nystagmus, abnormal extra-ocular movements, saccades and evidence of oculomotor apraxia or opsoclonus. Cranial nerve examination allows for thorough evaluation of brainstem and cerebellar function. Abnormal speech patterns may suggest brainstem or cerebellar dysfunction or could also reflect accompanying behavioral/developmental delay and/or anxiety.
Tone: Careful assessment of tone in multiple phases of activation is the initial step to a thorough motor exam in a child with disordered movements. Ideally, the child is observed at both rest and during activity. Tone can be particularly difficult to assess, especially in the child who has spasticity, dystonia, or dyskinesias. The initial approach in-
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volves a determination of whether the child has normal tone while fully at rest and whether that tone abnormality involves the extremities alone or in combination with the head/trunk. A child who appears stiff with high tone may actually have hypotonia with overlying spasticity, or relatively normal baseline tone with action-induced dystonia, or just be nervous and unable to relax. Usually, children with isolated dystonia do not have rigidity, cogwheeling, or elevated tone at rest and so these findings should be identified if present. Spasticity, with tone that increases with velocity, demonstrates spastic catch, and has resulted in contractures is more common. The distinction is important to narrowing a differential diagnosis, but often in hypertonic children there is a mixture of spasticity and dystonia.
Bulk: Assessment of bulk includes evaluating for atrophy and asymmetry. In contrast, increased bulk or muscle definition, which is atypical in young children, can be a sign of chronic muscle overactivity. This can be seen in children with dystonia due to excessive patterns of activation during routine movement. It also can indicate low subcutaneous fat stores secondary to chronic over-activity.
Strength: When manual muscle testing is not feasible due to the age of a child, strength can be assessed by monitoring the child during play. Can the child sit independently, holding his head steady? Can he stand and walk without assistance? Can he climb into his parent’s lap, run, jump, or lift toys above his head?
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Is the child quick to perform actions or does he need extra time to initiate movements? Does he perform movements efficiently using only the involved extremities or does he have excess movements in neighboring or contralateral muscle groups that interfere with execution of a desired task? Does he perform movements slowly or irregularly?
Sensory: Of note, the sensory exam can be unreliable in children. Minor discrepancies are commonly reported by children or adolescents with intact sensation and often times a detailed sensory exam is relatively low-yield in a child. In anxious children, the sensory exam can be particularly difficult and may contribute to worsened anxiety or new complaints. Thus, abnormalities on exam should be interpreted cautiously, and confirmed with repeat examination.
Cerebellum: Cerebellar examination is ongoing throughout the exam and includes eye movements, speech articulation and pacing, postural control, limb control, and gait. Additional evaluation for tremor is an important component of the movement exam. Coordination assessment and interpretation of findings are highly age dependent. In infants, observation of feeding can be very helpful. In older children use of small stacking blocks is helpful in demonstrating hand use and hand-eye coordination.
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Motor exam techniques for specific diagnoses: Distraction, play, and other similar techniques are especially helpful in enhancing and/or minimizing movements in question. For example, dystonia, chorea, tremor, and other movements may intensify when the patient is demonstrating the movement with intention, but can improve when the child is performing other tasks that utilize the same muscles, but is distracted from the problem by a toy or other engaging activity. In children with tics, it can be helpful during the exam to ask a child to demonstrate (and then suppress) his or her motor and/or vocal tics. Frequent tics can generally be shown to diminish or stop during purposeful movements of the same muscle groups. For children with suspected chorea, observe the child for restlessness while sitting quietly and check for exacerbation during actions. Also check for motor impersistence, the inability to sustain voluntary action, by having the child grip the examiner’s two fingers with their two hands simultaneously (where the impersistence and regripping is termed “milkmaid’s grip”) and protrude the tongue (where the impersistence causes the protruding tongue to dart in and out). In evaluation of dystonia look for unusual patterns of muscle co-contractions that cause jerking and posturing in a dynamic fashion, influenced differentially depending on the type of action including reaching, maintaining limbs extended in various postures, and walking. Be sure to check for subtle sensory tricks, also called gestes antagonistes. Attempt to provoke episodic dystonia in the office. When doing so, be careful to discern whether the patient has action-induced dystonia versus less commonly, paroxysmal ki-
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nesigenic dystonia. Watch carefully for evidence of involvement in other limbs or muscles beyond those reported by the patient. Evaluation of tremor should determine whether the tremor occurs at rest, which is a red flag for a hypokinetic rigid disease in children, versus with action; in particular, maintaining limbs outstretched for postural tremor and reaching repeatedly to a target for intention tremor. Document the anatomic distribution of the tremor and whether the tremor has a regular or irregular, jerky oscillation that varies with position. Use of an Archimedes spiral worksheet can help to quantify tremor. Activities such as pouring water into a cup and holding cup of water outstretched are also helpful in detecting tremor. Watch closely for tremor variability with distraction, hand position, or specific motor tasking as this can be especially helpful when narrowing your differential. Parkinsonism is rare in children but should not be missed. If rigidity or cogwheeling was noted on tone exam, it is helpful to videotape the hands at rest and to pay careful attention to facial expressiveness, and fluid initiation of movement and movement speed. Current and prior medication and/or drug exposure should always be considered when determining etiology of parkinsonism in a child. Psychogenic movements are very common in children and often (but not always) improve with distraction on exam. Psychogenic tremor, tics, and chorea may be entrainable. Nevertheless, it is equally important to note that anxiety is very common with organic movement problems and may contribute to waxing/waning symptoms making it more difficult to clearly identify an organic movement disorder. Regardless of etiology, many abnormal movements will worsen as anxiety heightens and conversely also improve with improvement in anxiety. Thus, it is prudent to be cautious when attributing a
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movement to psychogenic causes, particularly when the phenomenology is dystonic. Children often subconsciously embellish or disguise abnormal movements. This again highlights the importance of observation in multiple environments and emotional states to achieve and accurate diagnosis. Movement disorders in children are often mixed. For example, a child with chorea may also demonstrate accompanying dystonia. In these cases, it is helpful to first identify the movement that is most interfering with function. This approach will then further guide decision making for treatment and intervention. Movement rating scales can also be helpful and appropriate tools for evaluation and monitoring of symptoms in specific diseases.
Testing and observing parents and siblings during patient visit It is important to carefully observe parents and siblings when considering possible etiologies of abnormal movements in children. Essential tremor can be more easily diagnosed by performing a tremor exam for both parents and siblings. Parents may have an unrecognized history of prior and even current tics, dismissed in their own childhood as ‘habits.’ Mild dystonia may also go unrecognized or dismissed. If a child presents with writer’s cramp, observing handwriting samples from not only the child but also his parents can be essential to the diagnosis of an underlying primary dystonia.
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Multimedia exam: Accurate diagnosis from phenomenology is greatly aided by video exam when available [20, 35-37]. Further group review of video exam with colleagues with experience in movement disorders can be especially helpful in obtaining an accurate diagnosis. One unique advantage is the video exam serves to accurately capture a child’s exam at specific time intervals. Movement disorders that are particularly difficult to diagnose in real time can be captured on video and slowed down for careful assessment. Additionally, asking the parents for photos and old home videos can be particularly helpful in assessing episodic movements that are unobservable in the clinic or in the case of progressive decline in motor exam over time.
REACHING A DIAGNOSIS Refining a differential diagnosis for disordered movement in children: Movement specialists typically rely on a phenomenological approach to characterization of movement disorders in both adults and children [38-41]. Consideration of the complex motor circuitry involved in both normal and abnormal movements supports first using phenomenology (rather than anatomy) to classify and subdivide pediatric and adult movement disorders. A phenomenological approach relies on skilled pattern recognition on history and exam in order to identify the most likely diagnosis and helps distinguish between ataxia, athetosis, ballism, chorea, dystonia, myoclonus, parkinsonism, stereotypies, tics, and tremor. The most common pediatric movement disorders such as tics, stereotypies, developmental tremor, and abnormal movements associated
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with underlying static encephalopathy are typically quickly identifiable using a phenomenological approach. Often the phenomenology, when coupled with information from your detailed history in addition to the age and developmental state of the child, can quickly lead to a clear diagnosis, or will at least guide potential localization of the abnormal movements to a specific anatomic site. Additional anatomic localization may be dependent upon neuroimaging such as brain magnetic resonance imaging (MRI). The differential diagnosis can often be further narrowed once the history, time course, and age of patient at symptom onset are taken into consideration. It is important to remember the caveat that some movement disorders present differently in children compared to adults. Such detailed characterization of disease phenotype may assist in further determination of associated genotype, or at least aid in narrowing choices for initial genetic testing. In cases where phenomenology and history are not enough to make a clear diagnosis it is always important to rule out secondary causes considering etiologies such as drug/toxin use/exposure/ingestion/withdrawal, movements due to other neurologic diagnoses such as migraine or seizures, infection, inflammatory processes, vascular and traumatic etiologies, metabolic or mitochondrial disease, and other genetic conditions. For more complex diagnoses, experts in the field advocate for a stepwise, methodical assessment of phenomenology [20, 36] to further assess complex movement. We have outlined a phenomenological approach, as modified from previously published approaches [20, 39]. (Figure 3) Reviewing formal definitions of movement disorders can also be helpful [42-44].
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In the following articles of this special movement disorders edition of Seminars in Pediatric Neurology authors will guide you through differential diagnosis and details about a number of important diagnoses and pathologies in pediatric movement disorders ranging from very common childhood habits, stereotypes and tics, to much rarer neurologic conditions. Additional components of history taking and physical exam techniques and findings will be addressed according to the specific phenomenology discussed in each chapter.
Disclosure of interests: Dr. Gilbert has received honoraria and/or travel support from the Tourette Syndrome Association, the American Academy of Pediatrics, and the Child Neurology Society. He has received book royalties from Elsevier and Wolters Kluwer. He has received compensation for expert testimony for the U.S. D.O.J. D.V.I.C. program. Dr. Gilbert has received research support from the NIH (NIMH, NINDS). He has received funding for work as a clinical trial site investigator from Ecopipam Pharmaceuticals (clinical trial, Tourette Syndrome) and EryDel (clinical trial, Ataxia Telangiectasia).
The authors have no commercial, proprietary, or financial interest in any products or companies described in this article.
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Figure 1: Motor control develops in parallel with central and peripheral myelination, occurring in a rostro-caudal gradient accompanied by progressively diminishing primitive reflexes and carefully timed emergence of postural reflexes.
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Figure 2: A schematic representation of the major anatomical brain areas and functional pathways involved in each phase of voluntary movement. There are extensive feedback loops and overlap of signaling, as suggested by the high degree of overlap between brain areas designated in the figure.
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Figure 3: Schematic representation of the diagnostic approach to children with movement disorders.
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