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Management of the Spastic Wrist and Hand in Cerebral Palsy Nels D. Leafblad, BS, Ann E. Van Heest, MD CME INFORMATION AND DISCLOSURES The Review Section of JHS will contain at least 2 clinically relevant articles selected by the editor to be offered for CME in each issue. For CME credit, the participant must read the articles in print or online and correctly answer all related questions through an online examination. The questions on the test are designed to make the reader think and will occasionally require the reader to go back and scrutinize the article for details. The JHS CME Activity fee of $15.00 includes the exam questions/answers only and does not include access to the JHS articles referenced. Statement of Need: This CME activity was developed by the JHS review section editors and review article authors as a convenient education tool to help increase or affirm reader’s knowledge. The overall goal of the activity is for participants to evaluate the appropriateness of clinical data and apply it to their practice and the provision of patient care.

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Copyright ª 2015 by the American Society for Surgery of the Hand. All rights reserved.

    

Clarify the concept of neuroplasticity. Elucidate the clinical presentation of the wrist and hand among cerebral palsy patients. List classifications of upper extremity cerebral palsy. Examine the nonsurgical treatment including therapy for wrist and hand cerebral palsy. Discuss the surgical treatment and outcomes for the wrist and hand among cerebral palsy patients.

From the Department of Orthopaedic Surgery and the Medical School, University of Minnesota, Minneapolis, MN. Received for publication November 10, 2014; accepted in revised form November 20, 2014. No benefits in any form have been received or will be received related directly or indirectly to the subject of this article.

Corresponding author: Ann E. Van Heest, MD, Department of Orthopaedic Surgery, University of Minnesota, 2450 Riverside Ave., Ste. R200, Minneapolis, MN 55454; e-mail: [email protected]. 0363-5023/15/4005-0032$36.00/0 http://dx.doi.org/10.1016/j.jhsa.2014.11.025

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Research from the last 5 years on the pathophysiology and treatment of upper extremity sequelae of cerebral palsy (CP) is presented. The development of new treatments of CPaffected limbs, utilizing the brain’s inherent neuroplasticity, remains an area of promising and active research. Functional magnetic resonance imaging scans have evaluated the role of neuroplasticity in adapting to the initial central nervous system insult. Children with CP appear to have greater recruitment of the ipsilateral brain for motor and sensory functions of the affected upper limb. Studies have also shown that constraint-induced movement therapy

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results in localized increase in gray matter volume of the sensorimotor cortex contralateral to the affected arm targeted during rehabilitation. Recent therapy interventions have emphasized the role of home therapy programs, the transient effects of splinting, and the promise of constraint-induced movement therapy and bimanual hand training. The use of motion laboratory analysis to characterize the movement pattern disturbances in children with CP continues to expand. Classification systems for CP upper limb continue to expand and improve their reliability, including use of the House Classification, the Manual Ability Classification System, and the Shriner’s Hospital Upper Extremity Evaluation. Surgical outcomes have greater patients’ satisfaction when they address functional limitations, also in addition to aesthetics, which may improve patients’ self-esteem. Surgical techniques for elbow, wrist, fingers, and thumb continue to be refined. Research into each of these areas continues to expand our understanding of the nervous system insults that cause CP, how they may be modified, and how hand surgeons can continue to serve patients by improving their upper limb function and aesthetics. (J Hand Surg Am. 2015;40(5):1035e1040. Copyright  2015 by the American Society for Surgery of the Hand. All rights reserved.) Key words Cerebral palsy, stereognosis.

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HE PURPOSE OF THIS ARTICLE IS TO review literature from the last 5 years to update hand surgeons regarding the pathophysiology and treatment of upper extremity sequelae secondary to cerebral palsy (CP). By definition, CP is “a group of disorders of development of movement and posture causing activity limitations that are attributed to nonprogressive disturbances that occurred in the developing fetal or infant brain.”1 Etiologies can include fetal stroke, brain anoxia, central nervous system (CNS) infections, maternal infections, or CNS congenital malformations. Populationbased studies report prevalence estimates of CP ranging from 1.5 to 4 per 1,000 live births, which makes it the most common motor disability in childhood.2 Traditionally, the hand surgeon has treated the secondary peripheral manifestations of the primary CNS insult, because few CNS treatments exist. However, future treatments of upper extremity pathology due to CP may evolve by gaining a greater understanding of the primary CNS insults and CNS plasticity from such insults. Considerable work has been done in the last 5 years in attempt to better understand these processes regarding upper extremity use and function.

timing of the insult during development. Structural neuroplasticity has already been demonstrated in adult stroke patients undergoing neurorehabilitation. Several interventions are now being employed to increase upper limb function in children with unilateral CP. Inguaggiato et al3 found that successful noninvasive rehabilitative strategies, including constraint-induced movement therapy (CIMT) and virtual reality therapy, result in enlargement of the primary hand motor area contralateral to the paretic hand. Increased activation was also found in the contralateral sensory cortex, supplementary motor area, premotor cortex, and cerebellum. These plastic changes correlate with the enhancement of motor skills of the paretic upper limb. Eyre et al4 examined brain plasticity utilizing transcranial magnetic stimulation to characterize corticospinal tract development in healthy children, children with perinatal stroke with hemiplegia, and bilateral lesions. Magnetic resonance imaging (MRI) and anatomical studies showed that ipsilateral corticospinal axons from the noninfarcted hemisphere to the paretic side undergo compensatory hypertrophy. Such hypertrophy predicts severe impairment in the upper limb after 2 years. Similar to amblyopia, it appears that the increased projections from the ipsilateral cortex actually competitively displace the remaining projections from the contralateral (injured) cortex. Krageloh-Mann and Cans5 state that the healthy hemisphere plays an important role after unilateral insults. They confirm that, in the motor system, there is compensatory recruitment of ipsilateral tracts with limited functionality in the affected limb.

NEUROPLASTICITY The functional and structural changes that take place after insult to the CNS are part of a process referred to as adaptive plasticity. These changes occur in an attempt to offset or improve functions compromised by the pathological insult, whether they arise from malformations, ischemia, or parenchymal lesions. Mechanisms of plasticity differ depending on the J Hand Surg Am.

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Holmström et al6 have reported that, of the various lesions responsible for CP, the lesion associated with the most favorable hand function is white matter damage of immaturity, in which there is mild white matter loss and the presence of contralateral motor projections to the paretic hand. The most impaired hand function was observed in children with ipsilateral motor projections, regardless of the type of damage. In addition, van de Winckel et al7 examined brain activation patterns in children with unilateral CP compared to normally developing children during active and passive movement as well as tactile stimulation. They concluded that, in children with CP, there is an increased reliance on the ipsilateral brain for motor and sensory function to the paretic limb. Using MRI and transcranial magnetic stimulation, Mackey et al8 found decreased intracortical and interhemispherical inhibitory mechanisms in children with CP. More intact inhibition correlates with higher limb function. Hopefully, interventions can be developed that would enhance intracortical and interhemispherical inhibition in order to restore the excitatory balance in the brain in patients with CP. Such interventions are already being explored in the adult stroke population.

PATIENT EVALUATION Several studies in the last 5 years describe advances in motion laboratory assessment for evaluation of children with upper extremity CP. By definition, CP is a movement disorder, but the type of movement impairment may clinically manifest as spastic, flaccid, dystonic, or a combination thereof. In addition, the manifestations of CP may vary in the different segments of the limb: shoulder, elbow, forearm, wrist, fingers, and thumb. Fitoussi et al11 report using a specific kinematic protocol to measure the ability of hemiplegic patients with CP to carry out simple daily tasks before and after therapy with either botulinum toxin injection or surgery. The study found that, as problems in the forearm, wrist, and thumb were addressed and improved with therapy, so did the proximal kinematic problems. This suggests that proximal deficits could be related to compensatory movement strategies and/ or cocontractions and should be addressed secondarily after treatment of distal issues. Klotz et al12 report that motion analysis is a useful clinical tool for evaluating both coordination and range of motion limitations. They describe use of a fingertip reach task, in which the child touches the top of a bottle with the index fingertip followed immediately by touching the nose tip. This analysis shows movement deviations due to lack of coordination very clearly for children with CP. Jaspers et al’s study13 of spatiotemporal and kinematic parameters in 3-dimensional motion analysis revealed that children with hemiplegic CP have longer movement durations and less straight trajectories in upper extremity movements. Compared with normally developing children, children with CP also have more wrist flexion and less elbow extension and forearm supination during reach, reach to grasp, and gross motor tasks. In addition, children with CP have increased trunk movements and reduced shoulder elevation during reach activities. Motion laboratory analysis coupled with dynamic electromyography testing was used in tendon transfer surgery.14 Van Heest et al14 compared the preoperative and postoperative firing pattern of the flexor r

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constraining the less-affected upper limb with CIMT may lessen primary motor cortex activity controlling both upper limbs—a suboptimal therapy. Speculatively, bimanual training may be a more appropriate therapy for these children, but its efficacy may depend on interhemispherical connections.

Role of therapy based on neuroplasticity CIMT, a rehabilitative modality rooted in neuroplasticity, has been used for years in the adult population and has more recently been shown to improve upper extremity functionality in children with CP. Sterling et al9 found that CIMT resulted in localized increase in contralateral gray matter volume of the sensorimotor cortex during rehabilitation. In addition, increased gray matter volumes were observed in the ipsilateral sensorimotor cortex and contralateral hippocampus. There was a significant improvement in spontaneous use of the upper extremities in daily activities following CIMT. Although not yet proven, there seems to be a causal relationship between increases in gray matter volume and the magnitude of motor improvement. Gordon et al10 have suggested that there may be limitations to the utility of CIMT, particularly when there is early-onset damage. When ipsilateral projections from the unaffected hemisphere reorganize and are strengthened to the paretic hand, and contralateral projections are weakened, the patients typically have more adversely affected hand function. The earlier the onset of the damage, the greater the reorganization that occurs. In children with substantial ipsilateral corticospinal tract reorganization, J Hand Surg Am.

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carpi ulnaris (FCU) in children treated with an FCUe toeextensor carpi radialis brevis tendon transfer. Before surgery, the most common pattern seen was activation of the FCU during grasp and relaxation of the FCU during release. This pattern did not change in 6 out of 7 patients after surgery, suggesting that the FCU does not change phase after its transfer.

TABLE 1. Manual Ability Classification System (http://www.macs.nu/)

Classification systems Early detection and classification of hand abnormalities in CP can guide operative and nonoperative therapies. Various classification systems are available for this process. The Manual Abilities Classification System (MACS) (Table 1) is a commonly used tool and evaluates the child’s ability to handle objects in daily activities. The House functional classification15 is useful in describing grip function in each hand separately. The Zancolli classification of active finger and wrist extension, along with the spastic thumbin-palm deformity classification of House, estimates dynamic spasticity of the hand. A recent article evaluated hand function in 367 children using these common classification systems.16 Gajewska et al17 used the MACS system and noted that the presence of epilepsy in children with CP is associated with worse manual function, limitations in conscious motor functions, and increased mental impairment. Compagnone et al18 compared the gross motor function classification system, expanded and revised, the MACS, and the Communication Function Classification System as 3 systems that are used to classify functional levels of children with CP. These 3 systems correlate strongly with one another and complement each other in describing the complete functional profile of CP. In addition, an intelligence quotient test seems to influence the global functional profile of CP patients. Another classification schedule has been developed to allow clinicians to assess spontaneous function, dynamic positioning, and child’s ability to perform grasp-release maneuvers. This is known as the Shriners Hospital for Children Upper Extremity Evaluation (SHUEE), a validated videobased tool.19

Level I

Handles objects easily

II

Handles objects with reduced quality and speed

III

Handles objects with difficulty requiring modification

IV

Handles objects only in adapted situations

V

Does not handle objects

movements, and a substantial amount of time is spent in training. When considering the various noninvasive interventions for unilateral upper extremity CP, Taub and Uswatte21 suggest that CIMT and bimanual training have demonstrated the most efficacy and clinical practicality for improving functionality. Both papers advocate continuing at-home therapy to maximize clinical improvement. Jackman et al,22 in a systematic meta-analysis, evaluated the effectiveness of hand orthoses in children with CP. Although they found that the use of hand orthoses in addition to therapy may offer a small benefit for manual skill development, this effect diminishes 2 to 3 months after discontinuation of orthosis use. Orthoses can create discomfort and cosmetic problems. Consideration of these factors should influence the clinical appropriateness of orthosis use. Further methodical research is necessary to determine the overall effectiveness of hand orthoses to improve outcomes. A randomized, double-blind, placebo-controlled study by Koman et al23 evaluated the short-term effects of botulinum toxin injections for treatment of upper extremity spasticity in children with CP. Study participants underwent an average of 3 injections based on their individual spasticity patterns. A higher percentage of children treated with botulinum toxin injections showed improvement in the Melbourne assessment after 6 months when compared with children receiving placebo. They concluded that, when surgery is not indicated, repeated botulinum A toxin injections are safe and efficacious in providing short-term functional improvement of children’s upper extremity spasticity.

NONSURGICAL TREATMENT AND OUTCOMES Nonsurgical treatment options for the upper extremity in CP have primarily focused on physical therapy, splinting, and botulinum toxin injections. Sakzewski et al20 recently reported that the most effective rehabilitative programs have several elements in common: therapy is goal directed, measureable goals are identifiable by children and caregivers, motor training is focused on activities rather than individual J Hand Surg Am.

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SURGICAL TREATMENT AND OUTCOMES Two treatment outcomes that have not often been evaluated in surgical treatment of the CP upper extremity are self-esteem and aesthetics. Riad et al24 have advocated that health care providers should take into r

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elbow flexion contractures,29,30 swan neck deformities,31 and thumb-in-palm deformity.32 An algorithm for treatment of elbow flexion contractures has been outlined by Carlson and Carlson.31 The amount of preoperative contracture must be accounted for when determining the extent of elbow muscle lengthening. In this study, patients with fixed elbow deformities less than 45 underwent partial lengthening, whereas those with fixed deformities greater than 45 underwent full release. A direct correlation exists between increasing age and the degree of preoperative contracture; patients 12 years of age or older are 5.5 times as likely to have fixed contracture (passive extension  45 ) than patients younger than 12 years of age. The appropriate surgical treatment, based on the degree of preoperative contracture, can greatly improve elbow flexion posture angle at ambulation, active and passive extension, and total range of motion. Van Heest32 described use of thumb adductor release, extensor pollicis longus rerouting and metacarpophalangeal stabilization procedures depending on the preoperative thumb-in-palm deformity. Research from the last 5 years on the pathophysiology and treatment of CP upper extremity sequelae is presented in this update article. Functional MRI scans have evaluated the role of neuroplasticity in adapting to the initial CNS insult. Children with CP appear to have greater recruitment of the ipsilateral brain for motor and sensory function of the affected upper limb. Studies have also shown that CIMT results in localized increases in gray matter volume of the sensorimotor cortex contralateral to the affected arm targeted during rehabilitation. The development of new treatments of CP-affected limbs, utilizing the brain’s inherent neuroplasticity, remains an area of promising and active research. Recent reviews of therapy interventions have emphasized the role of therapy extending into home programs, the transient effects of fabricating an orthosis, and the promise of CIMT and bimanual hand training. The use of motion laboratory analysis to characterize the movement pattern disturbances present in children with CP continues to expand. Classification systems for upper limb involvement due to CP continue to expand and improve their reliability, including use of the House classification,15 the MACS, and the SHUEE. Outcomes after surgery have been reported to have greater patient satisfaction when they address not only functional limitations but also aesthetics, which may improve patients’ selfesteem. Lastly, surgical techniques continue to be refined for treatment of the elbow, wrist, fingers, and thumb. Continued research into each of these areas

account the mental health of patients with CP when making treatment decisions. Although movement deviations in upper and lower extremities often occur simultaneously in patients with unilateral CP, the authors report that upper extremity deviations correlate most with lower self-esteem. Even in high-functioning patients with mild CP, self-esteem may be adversely affected by such deviations. Elbow flexion deformity is the main contributor to decreased self-esteem, when compared with shoulder flexion, shoulder abduction, and wrist flexion deformity. Similarly, Makki et al25 have reported that cosmetic appearance after surgical correction may have a greater influence on patient’s satisfaction than functional outcome. Older children (> 12 y) are more self-conscious about the appearance of their hand. These authors suggest that it is important not to underestimate the psychosocial implications of hand deformity. Libberecht et al26 reported that patient satisfaction is significantly higher in patients with considerable cosmetic improvement after surgery. It is not unreasonable to suspect that patients may be seeking treatment primarily for cosmetic reasons. As such, even if surgical intervention is not expected to deliver considerable functional improvement, correcting the deformity for cosmetic reasons can be a worthwhile endeavor for the patient. Gong et al27 have reported on the use of the MACS to categorize outcomes after surgery. They reported that, by dichotomizing the MACS into high and low levels for baseline hand function prior to surgery, one can effectively predict surgical outcome, regardless of the specific type of surgery performed. Although patients in both groups experience substantial improvement, patients with high MACS levels have greater improvements in function (utilizing the House functional scale) and overall satisfaction, but less improvement in hygiene status compared with those with low MACS levels. Using the SHUEE to assess therapeutic outcomes, Smitherman et al28 found that single-event multilevel surgery for children with hemiplegic CP can significantly improve thumb, finger, wrist, and forearm segmental positioning as well as spontaneous function, but does not significantly change grasp-release ability. In addition, the single-event multilevel surgical approach provides the patients and families with the benefits of avoiding staged surgical interventions. The SHUEE has been demonstrated to be reliable in clinical decision making and in assessment of functional outcomes after surgery. Other specific surgical technique articles and their results have been published regarding treatment of J Hand Surg Am.

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continues to expand our understanding of the CNS insults that cause CP, how they may be modified, and how we, as hand surgeons, can continue to serve our patients to improve their upper limb function and esthetics.

16. Arner M, Eliasson AC, Nicklasson S, Sommerstein K, Hagglund G. Hand function in cerebral palsy. Report of 367 children in a population-based longitudinal health care program. J Hand Surg Am. 2008;33(8):1337e1347. 17. Gajewska E, Sobieska M, Samborski W. Associations between manual abilities, gross motor function, epilepsy, and mental capacity in children with cerebral palsy. Iran J Child Neurol. 2014;8(2): 45e52. 18. Compagnone E, Maniglio J, Camposeo S, et al. Functional classifications for cerebral palsy: correlations between the Gross Motor Function Classification System (GMFCS), the Manual Ability Classification System (MACS) and the Communication Function Classification System (CFCS). Res Dev Disabil. 2014;35(11): 2651e2657. 19. Davids JR, Peace LC, Wagner LV, Gidewall MA, Blackhurst DW, Roberson WM. Validation of the Shriners Hospital for Children Upper Extremity Evaluation (SHUEE) for children with hemiplegic cerebral palsy. J Bone Joint Surg Am. 2006;88(2):326e333. 20. Sakzewski L, Ziviani J, Boyd RN. Efficacy of upper limb therapies for unilateral cerebral palsy: a meta-analysis. Pediatrics. 2014;133(1): e175ee204. 21. Taub E, Uswatte G. Importance for CP rehabilitation of transfer of motor improvement to everyday life. Pediatrics. 2014;133(1): e215ee217. 22. Jackman M, Novak I, Lannin N. Effectiveness of hand splints in children with cerebral palsy: a systematic review with meta-analysis. Dev Med Child Neurol. 2014;56(2):138e147. 23. Koman LA, Smith BP, Williams R, et al. Upper extremity spasticity in children with cerebral palsy: a randomized, double-blind, placebocontrolled study of the short-term outcomes of treatment with botulinum A toxin. J Hand Surg Am. 2013;38(3):435e446.e1. 24. Riad J, Brostrom E, Langius-Eklof A. Do movement deviations influence self-esteem and sense of coherence in mild unilateral cerebral palsy? J Pediatr Orthop. 2013;33(3):298e302. 25. Makki D, Duodu J, Nixon M. Prevalence and pattern of upper limb involvement in cerebral palsy. J Child Orthop. 2014;8(3): 215e219. 26. Libberecht K, Sabapathy SR, Bhardwaj P. The relation of patient satisfaction and functional and cosmetic outcome after correction of the wrist flexion deformity in cerebral palsy. J Hand Surg Eur Vol. 2011;36(2):141e146. 27. Gong HS, Chung CY, Park MS, Shin HI, Chung MS, Baek GH. Functional outcomes after upper extremity surgery for cerebral palsy: comparison of high and low manual ability classification system levels. J Hand Surg Am. 2010;35(2):277e283.e1e3. 28. Smitherman JA, Davids JR, Tanner S, et al. Functional outcomes following single-event multilevel surgery of the upper extremity for children with hemiplegic cerebral palsy. J Bone Joint Surg Am. 2011;93(7):655e661. 29. Gong HS, Cho HE, Chung CY, Park MS, Lee HJ, Baek GH. Early results of anterior elbow release with and without biceps lengthening in patients with cerebral palsy. J Hand Surg Am. 2014;39(5): 902e909. 30. Carlson MG, Hearns KA, Inkellis E, Leach ME. Early results of surgical intervention for elbow deformity in cerebral palsy based on degree of contracture. J Hand Surg Am. 2012;37(8): 1665e1671. 31. Carlson EJ, Carlson MG. Treatment of swan neck deformity in cerebral palsy. J Hand Surg Am. 2014;39(4):768e772. 32. Van Heest AE. Surgical technique for thumb-in-palm deformity in cerebral palsy. J Hand Surg Am. 2011;36(9):1526e1531.

REFERENCES

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1. Bax M, Goldstein M, Rosenbaum P, et al. Proposed definition and classification of cerebral palsy, April 2005. Dev Med Child Neurol. 2005;47(8):571e576. 2. Winter S, Autry A, Boyle C, Yeargin-Allsopp M. Trends in the prevalence of cerebral palsy in a population-based study. Pediatrics. 2002;110(6):1220e1225. 3. Inguaggiato E, Sgandurra G, Perazza S, Guzzetta A, Cioni G. Brain reorganization following intervention in children with congenital hemiplegia: a systematic review. Neural Plast. 2013;2013:356275. 4. Eyre JA, Smith M, Dabydeen L, et al. Is hemiplegic cerebral palsy equivalent to amblyopia of the corticospinal system? Ann Neurol. 2007;62(5):493e503. 5. Krageloh-Mann I, Cans C. Cerebral palsy update. Brain Dev. 2009;31(7):537e544. 6. Holmström L, Vollmer B, Tedroff K, et al. Hand function in relation to brain lesions and corticomotor-projection pattern in children with unilateral cerebral palsy. Dev Med Child Neurol. 2010;52(2): 145e152. 7. Van de Winckel A, Klingels K, Bruyninckx F, et al. How does brain activation differ in children with unilateral cerebral palsy compared to typically developing children, during active and passive movements, and tactile stimulation? An fMRI study. Res Dev Disabil. 2013;34(1):183e197. 8. Mackey A, Stinear C, Stott S, Byblow WD. Upper limb function and cortical organization in youth with unilateral cerebral palsy. Front Neurol. 2014;5:117. 9. Sterling C, Taub E, Davis D, et al. Structural neuroplastic change after constraint-induced movement therapy in children with cerebral palsy. Pediatrics. 2013;131(5):e1664ee1669. 10. Gordon AM, Bleyenheuft Y, Steenbergen B. Pathophysiology of impaired hand function in children with unilateral cerebral palsy. Dev Med Child Neurol. 2013;55(Suppl):432e437. 11. Fitoussi F, Diop A, Maurel N, Laasel el M, Ilharreborde B, Pennecot GF. Upper limb motion analysis in children with hemiplegic cerebral palsy: proximal kinematic changes after distal botulinum toxin or surgical treatments. J Child Orthop. 2011;5(5):363e370. 12. Klotz MC, van Drongelen S, Rettig O, et al. Motion analysis of the upper extremity in children with unilateral cerebral palsy—an assessment of six daily tasks. Res Dev Disabil. 2014;35(11):2950e2957. 13. Jaspers E, Desloovere K, Bruyninckx H, et al. Three-dimensional upper limb movement characteristics in children with hemiplegic cerebral palsy and typically developing children. Res Dev Disabil. 2011;32(6):2283e2294. 14. Van Heest A, Stout J, Wervey R, Garcia L. Follow-up motion laboratory analysis for patients with spastic hemiplegia due to cerebral palsy: analysis of the flexor carpi ulnaris firing pattern before and after tendon transfer surgery. J Hand Surg Am. 2010;35(2): 284e290. 15. House JH, Gwathmey FW, Fidler M. A dynamic approach to the thumb-in-palm deformity in cerebral palsy. J Bone Joint Surg Am. 1981;63(2):216e225.

J Hand Surg Am.

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Management of the spastic wrist and hand in cerebral palsy.

Research from the last 5 years on the pathophysiology and treatment of upper extremity sequelae of cerebral palsy (CP) is presented. The development o...
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