Limb Preference in Children with Obstetric Brachial Plexus Palsy

Limb Preference in Children with Obstetric Brachial Plexus Palsy

Limb Preference in Children with Obstetric Brachial Plexus Palsy Lynda J.-S. Yang, MD, PhD*, Praveen Anand, MD†, and Rolfe Birch, MD‡ Brachial plexus ...

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Limb Preference in Children with Obstetric Brachial Plexus Palsy Lynda J.-S. Yang, MD, PhD*, Praveen Anand, MD†, and Rolfe Birch, MD‡ Brachial plexus palsy affects children differently than adults. In children with obstetric brachial plexus palsy, motor development must depend on nervous system adaptation. Previous studies report sensory plasticity in these children. This noninvasive study provides support for neural plasticity (the general ability of the brain to reorganize neural pathways based on new experiences) in children with obstetric brachial plexus palsy by considering upper limb preference. As in the general population, we expect that 90% of children would prefer their right upper limb. However, only 17% of children affected by right obstetric brachial plexus palsy prefer the right upper limb for overall movement; children with left obstetric brachial plexus palsy did not significantly differ from the general population in upper limb preference. This study also provides the first evidence of a significant correlation between actual task performance and select obstetric brachial plexus palsy outcome measurement systems, thereby justifying the routine use of these outcome measurement systems as a reflection of the practical utility of the affected limb to the patient. © 2005 by Elsevier Inc. All rights reserved. Yang LJS, Anand P, Birch R. Limb preference in children with obstetric brachial plexus palsy. Pediatr Neurol 2005; 33:46-49.

in children affected by obstetric brachial plexus palsy is also evidenced in the perfect localization of restored sensation in avulsed spinal root dermatomes after nerve transfer from a distant spinal region [1]. This study attempts to provide further support for neural plasticity (the general ability of the brain to reorganize neural pathways based on new experiences) in children with obstetric brachial plexus palsy by investigating limb preference: because the majority of the population prefers to use the right upper limb, a shift to left upper limb preference by the majority of the patients would be consistent with plastic adaptation of neural pathways to perinatal deafferentation injury. Functional assessment of limb preference for gross and fine task movements demonstrates both the pragmatic use of the affected limb and the realistic utility of the affected limb to the child. Frequent extensive task assessments can be cumbersome and impractical, so the use of outcome measurement systems (based on the extent of movement at the joints) to assess limb function is common. Accurate reflection of actual limb function by these outcome measurement systems has not been studied, and this issue is also addressed in the present investigation.

Clinical Materials and Methods Patients

Introduction Limb preference in children with obstetric brachial plexus palsy (OBPP) has wide implications for the development of the child. Nervous system adaptation in these children is expressed through the striking lack of referred sensation and chronic pain avulsion syndromes, as opposed to adults who suffer these sequelae of brachial plexus injury. Plasticity of the nervous system

Because children who experienced excellent recovery and hospital discharge before age 5 were usually lost to follow-up, all patients between the ages of 5 and 9 diagnosed with obstetric brachial plexus palsy and who had routinely scheduled clinic visits were included in the study. The children in this study were retained because of continuing issues such as shoulder deformity. The age range was chosen to allow for adequate maturity to cooperate with the assessment. Patients were excluded if other medical conditions prohibited participation in the clinical tests for determination of limb dominance.

From the *Department of Neurosurgery, University of Michigan Health System, Ann Arbor, Michigan, USA; †Peripheral Neuropathy Unit, Imperial College School of Medicine, Hammersmith Hospital, London, UK; and ‡Peripheral Nerve Injury Unit, Royal National Orthopaedic Hospital, Stanmore, Middlesex, UK.

Communications should be addressed to: Dr. Yang; Department of Neurosurgery; University of Michigan Health System; 1500 E. Medical Center Drive; Room 3552 TC; Ann Arbor, MI 48109-0338. Received October 6, 2004; accepted January 31, 2005.

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© 2005 by Elsevier Inc. All rights reserved. doi:10.1016/j.pediatrneurol.2005.01.011 ● 0887-8994/05/$—see front matter

Table 1. Correlation of degree of upper limb preference with outcome measurement systems

Narakas classification Mallett Gilbert (modified) Elbow Raimondi

Gross Movement

Fine Movement

r ⫽ 0.488 P ⫽ 0.002 r ⫽ 0.460 P ⫽ 0.004 Not significant r ⫽ 0.362 P ⫽ 0.028 r ⫽ 0.350 P ⫽ 0.034

r ⫽ 0.495 P ⫽ 0.002 r ⫽ 0.376 P ⫽ 0.022 Not significant Not significant r ⫽ 0.394 P ⫽ 0.016

Abbreviations P ⫽ Significance (2-tailed) r ⫽ Correlation coefficient

Functional Limb Preference Assessment The test questionnaire for upper limb, lower limb, and eye dominance was based on the “Questionnaire for the Evaluation of Handedness” by Sattler [2]. Questions included the assessment of spontaneous activities with one and two hands, activities influenced by imitation and education, and activities shaped by the design of certain equipment. Task performance was witnessed by one of the authors. The average number of questions answered and activities performed by the children for fine movements was nine (e.g., threading string through bead, writing, picking up small beads), for gross movements 25 (e.g., holding large objects, opening a door, raising hand while in class), for a total of 34 questions. Eye and lower limb preference was assessed by three tasks for each modality. Additionally, part of the questionnaire polled the patient’s family members for handedness.

Motor Assessment We used four outcome measurement systems [3]. Shoulder function was assessed with the Mallett system [4]. A modified version of Gilbert’s classification (based solely on shoulder abduction and lateral rotation) was used to complement the Mallett system for shoulder function [5]. Elbow function was assessed using the system developed by Gilbert and Raimondi [6]. Hand function was assessed using Raimondi’s classification [7].

Statistical Methods Comparison of the test groups with the population was performed using the z test for a single proportion. The degree of limb preference was calculated as a ratio of the percentage of questions/tasks answered with the preferred limb over that of the contralateral limb. Spearman rank correlations were calculated between the degree of right/left handedness and the outcome measurement scores using SPSS for Windows, Version 10, released 2001 (SPSS Inc., 1989-2000). The correlations and their statistical significance are reported in Table 1.

Results Table 2 summarizes the patient data. Table 3 presents the overall limb preference of the population, the relatives of the subjects, the children with left obstetric brachial plexus palsy, and those with right obstetric brachial plexus palsy. The proportion of right-handers in those with right obstetric brachial plexus palsy was 4 of 23 (17%). This

percentage represents a significant difference in upper limb preference in these children when compared with the population proportion of 0.9 (z ⬎ 10, P ⬍ 0.001 using z test for a single proportion). However, there was no significant difference detected between the upper limb preference of the population and that of the children with left obstetric brachial plexus palsy. Table 1 presents the correlation of limb preference for gross and fine movements with the Narakas group and four outcome measurement systems. The degree of limb preference for both gross and fine movements reveals significant correlation with the Narakas classification. The measurement of hand function [7] significantly correlates with fine movements, whereas the measurement of elbow function significantly correlates with gross movements. Two measurements of shoulder function were assessed for correlation with upper limb preference. The Mallett scoring system yields significant correlation, whereas our modification of the Gilbert system reveals no significant correlation with upper limb preference. Furthermore, no significant correlation exists between eye or lower limb preference and upper limb preference, or with any of the outcome measurement systems.

Discussion Right limb preference is estimated in 90% of the population in both children and adults [8-10]. In this study, an estimate of the population hand preference, assessed by polling the relatives of the children in the study, was 87% right preference. During normal development, the adult pattern of hand preference becomes evident as early as 6 to 10 months, and is thought to be firmly established between the ages of 4 and 10 [11-14]. We assessed children from the ages of 5 to 9 because younger children would have difficulty cooperating with the assessment. In children with left obstetric brachial plexus palsy, 93% of the children preferred the right upper limb for overall movements, demonstrating no significant difference when compared with the population (e.g., there was no significant increase in right upper limb preference relative to the population). However, in children with right obstetric brachial plexus palsy, only 17% preferred to use their right upper limb for overall movements (z ⬎ 10, P ⬍ 0.001); the children were not divided into subgroups, because those in the better prognostic categories were less likely to undergo operation. If the majority of these children had not suffered traction injury to the right brachial plexus, they would have preferred their right upper limb. The ability to change to left upper limb preference may result from the brain’s ability to reorganize neural pathways on the basis of new experiences in these children. In contrast, the etiology of the lack of neural plasticity in children with left obstetric brachial plexus palsy demonstrated in this study merits further investigation.

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Table 2.

OBPP patient data

Pt. No. Right OBPP 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 20 21 22 23 Left OBPP 24 25 26 27 28 29 30 31 32 33 34 35 36 37

General Characteristics BP Age Repair? (yr) Sex

Level of Injury Narakas Group

Mallett

Gilbert

Raimondi

% Questions* for Gross Movement

% Questions* for Fine Movement

Elbow

Left

Right

Left

Right

Motor Assessment

N N N N N N Y Y N Y Y Y Y N N Y N N N Y Y Y Y Y

5 5 7 6 5 8 6 6 9 7 7 5 7 4 8 8 5 6 7 4 4 7 7 6

M F M F M F M M M F F F M M F M F F M M M F M M

1 1 1 1 1 1 1 1 2 2 2 2 2 3 3 3 3 3 4 4 4 4 4 4

14 14 14 12 15 15 13 14 13 11 13 13 14 11 13 10 13 14 13 14 14 11 4 10

3⫹ 2⫹ 5⫹ 3⫹ 6 5⫹ 1⫹ 4⫹ 1⫹ 3⫹ 3⫹ 3⫹ 5⫹ 2⫹ 4⫹ 5 3 3⫹ 3⫹ 3⫹ 3⫹ 2 1 6

5 5 5 5 5 5 5 4 5 3 5 5 5 4 5 3 4 4 2 4 4 2 2 1

5 5 5 3 5 5 5 2 4 3 5 5 5 4 5 2 5 5 3 3 3 4 1 2

86 62 56 100 100 96 96 16 95 92 96 96 96 87 100 100 100 46 100 100 100 96 100 96

32 71 78 0 14 7 8 100 5 8 4 4 4 13 18 7 8 54 9 0 0 4 0 4

63 63 20 89 100 80 100 0 33 100 50 100 90 63 100 100 100 36 100 100 100 100 100 100

38 63 90 11 0 30 0 100 67 0 50 0 10 38 0 10 0 64 0 0 0 0 0 0

N N N N N N N N Y Y Y Y Y Y

6 7 6 7 6 4 6 8 6 6 7 7 9 8

M F F M F M F F F M M F F M

1 1 1 2 2 2 2 2 3 4 4 4 4 4

15 14 15 15 12 14 15 12 11 11 9 10 10 8

3 4⫹ 6 5⫹ 4⫹ 3⫹ 5⫹ 3⫹ 1⫹ 1 4⫹ 1 2⫹ 1

5 5 5 5 5 5 5 5 3 3 3 4 2 3

5 5 5 5 4 5 5 5 3 4 3 3 2 3

43 10 16 4 85 52 20 5 8 0 0 7 4 10

100 90 87 100 58 93 92 100 100 96 100 96 100 100

30 33 0 0 25 40 20 0 0 0 0 0 13 0

100 100 100 100 88 90 100 100 100 100 100 100 100 100

Abbreviations BP ⫽ Brachial plexus N ⫽ No OBPP ⫽ Obstetric brachial plexus palsy Y ⫽ Yes * Total percentage may exceed 100% if some tasks were performed by both left and right hands.

Evidence for plasticity of the nervous system in children with obstetric brachial plexus palsy has been reported previously [1]. In cases of significant injury with poor neurophysiologic prognostication without spontaneous recovery by 3 months, surgical intervention (nerve transfer for avulsion injuries and nerve grafting for trunk injuries) to restore sensorimotor function was performed. Not only was excellent sensory function restored, but there was also perfect localization of the restored sensation in avulsed spinal root dermatomes, presumably routed via nerves that had been transferred from a distant spinal region.

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Although there are notable differences in clinical sensorimotor recovery between adults and children [3,15], evidence for nervous system plasticity also exists in adults suffering deafferentation injury [16,17]. For example, the degree of cortical reorganization seems to be correlated with the severity of phantom pain after limb amputation [18]. Consistent with this finding, other investigators report that subjects with congenital absence of a limb who did not experience phantom pain did not manifest cortical reorganization [19]. Increasing degree of affected limb preference for overall movements significantly correlates with less severe

Table 3.

Overall limb preferences

Population Patient relatives Left OBPP Right OBPP

Right Limb Preferred

Left Limb Preferred

90% 87% 93% 17%

10% 13% 7% 83%

Abbreviation OBPP ⫽ Obstetric brachial plexus palsy

groups (I and II) in the Narakas classification of obstetric brachial plexus palsy [20], which purports to provide a likely outcome for obstetric brachial plexus palsy patients based on the clinical determination of injured nerves. Likewise, increasing degrees of preference for using the affected limb for fine movements rather than gross movements correlates better with the Raimondi hand outcome measurement score, which is based on flexion/extension of the fingers and wrist and pronation/supination of the forearm [7]. The degree of limb preference for gross movements significantly correlates with Gilbert and Raimondi’s classification of elbow recovery based on flexion/ extension at the elbow, and Mallett’s assessment of movement at the shoulder significantly correlates with both gross and fine movements. No significant correlation was observed between the degree of limb preference and our modified version of Gilbert’s classification of the shoulder, which is based solely on abduction and lateral rotation. This report presents the first significant correlation between actual task performance and two of the three tested obstetric brachial plexus palsy outcome measurement systems (based on the extent of movement at different joints of the upper limb). We support the routine use of select outcome measurement systems as a reflection of the practical utility of the affected limb to the patient. References [1] Anand P, Birch R. Restoration of sensory function and lack of long-term chronic pain syndromes after brachial plexus injury in human neonates. Brain 2002;125:113-22. [2] Sattler J. Das linkshändige Kind in der Grundschule. Auer Verlag, Donauwörth, 12. Auflage 2005:19-21. [3] Birch R, Bonney G, Wynn Parry CB. Birth lesions of the

brachial plexus. In: Birch R, Bonney G, Wynn Parry CB, eds. Surgical disorders of the peripheral nerves. Edinburgh: Churchill Livingstone, 1998:209-33. [4] Mallett J. Paralysie obstetricale du plexus brachial. Rev Chir Orthop 1972;58:115-204. [5] Gilbert A. Obstetrical brachial plexus palsy. In: Tubiana R, ed. The hand. Vol. 4. Philadelphia: Saunders, 1993:576-601. [6] Gilbert A, Raimondi P. Evaluation of results in obstetric brachial plexus palsy. The elbow. Presented at the International Meeting on Obstetric Brachial Plexus Palsy, Heerlen, Germany, 1996. [7] Raimondi P. Evaluation of results in obstetric brachial plexus palsy. The hand. Presented at the International Meeting on Obstetric Brachial Plexus Palsy, Heerlen, Germany, 1993. [8] Giagazoglou P, Fotiadou E, Angelopoulou N, Tsikoulas J, Tsimaras V. Gross and fine motor skills of left-handed preschool children. Percept Mot Skills 2001;92:1122-8. [9] Penso D. On the other hand. Therapy Weekly 1996;22:11-2. [10] Peters M. Incidence of left-handed writers and the inverted writing position in a sample of 2194 German elementary school children. Neuropsychologia 1986;24:429-33. [11] Brown T, Cupido C, Scarfone H, Pape K, Galea V, McComas A. Developmental apraxia arising from neonatal brachial plexus palsy. Neurology 2000;55:24-30. [12] el-Mallakh RS, Wyatt RJ, Looney SW. Does motor cerebral dominance develop secondary to sensory dominance? Percept Mot Skills 1993;76:647-52. [13] Erhardt R. Developmental hand dysfunction: Theory, assessment, and treatment, 2nd ed. San Antonio: Therapy Skill Builders, a Division of The Psychological Corporation; translated into Japanese (1988), Tokyo, Japan: Ishiyaku Publishers. 1982, 1994:15. [14] Geschwind N, Galaburda AM. Cerebral lateralization. Biological mechanisms, associations, and pathology: I. A hypothesis and a program for research. Arch Neurol 1985;42:428-59. [15] Berman JS, Birch R, Anand P. Pain following human brachial plexus injury with spinal cord root avulsion and the effect of surgery. Pain 1998;75:199-207. [16] Halligan PW, Marshall JC, Wade DT, Davey J, Morrison D. Thumb in cheek? Sensory reorganization and perceptual plasticity after limb amputation. Neuroreport 1993;4:233-6. [17] Ramachandran VS, Stewart M, Rogers-Ramachandran DC. Perceptual correlates of massive cortical reorganization. Neuroreport 1992;3:583-6. [18] Flor H, Elbert T, Knecht S, et al. Phantom-limb pain as a perceptual correlate of cortical reorganization following arm amputation. Nature 1995;375:482-4. [19] Montoya P, Ritter K, Huse E, et al. The cortical somatotopic map and phantom phenomena in subjects with congenital limb atrophy and traumatic amputees with phantom limb pain. Eur J Neurosci 1998;10:1095-102. [20] Narakas AO. Obstetrical brachial plexus injuries. In: Lamb DW, ed. The paralysed hand. Edinburgh: Churchill Livingstone, 1987: 116-35.

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