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Clinical assessment, MRI, and EMG in congenital brachial plexus palsy
Clinical Assessment, MRI, and EMG in Congenital Brachial Plexus Palsy ¨ ge, MD‡, Nur Aydınlı, MD*, Kutluhan Yılmaz, MD*, Mine C ¸ alıs¸kan, MD†, Emre O ¨ zmen, MD* Mehtap Tunacı, MD§, and Meral O Thirteen infants with congenital brachial plexus palsy (eight with upper, five with upper and lower) were monitored by magnetic resonance imaging (the first performed between 7 and 41 days of age and the second at 3 months of age), electromyography (the first performed between 27 and 50 days and the second at 3 months), and the muscle scoring system of the Hospital for Sick Children (at 3, 6, and 9 months of age). The findings were evaluated with respect to the clinical status of the patients at 12 months of age. Magnetic resonance imaging, which could be performed readily even in the neonatal period, revealed pseudomeningoceles in two of the five patients with a poor prognosis (in all planes even in the early days after birth) and in two of the eight patients with a good prognosis (more easily visible at 3 months of age). Electromyography implied root avulsion in three of five patients with a poor prognosis. Electromyography can be of great value for patients with a poor prognosis and root avulsion but may underestimate the severity. The muscle scoring system (Hospital for Sick Children) was determined to be the most predictive method for prognosis. © 1999 by Elsevier Science Inc. All rights reserved. ¨ ge E, Aydınlı N, Tunacı M, Yılmaz K, C ¸ alıs¸kan M, O ¨ zmen M. Clinical assessment, MRI, and EMG in conO genital brachial plexus palsy. Pediatr Neurol 1999;21: 705-710.
births) has not decreased during the past 20 years [1,2]. Although CBPP has long been recognized as a health problem, prognosis data about CBPP in published reports are not clear enough. Most patients with CBPP improve spontaneously or with physical therapy, although some require additional treatment, such as neurosurgery. However, the best methods to assess the severity of the plexus lesions and to predict candidates for neurosurgical intervention and their outcomes are still controversial. Many clinical and laboratory approaches have been recommended. Gilbert et al. [3,4] proposed improvement in the flexion of the biceps muscle as a criterion of resolution, and Laurent et al. [5] suggested using the biceps, triceps, and deltoid muscles. Michelow et al. [6] and Clarke and Curtis [7] advocated using several other muscles. Some investigators [4,8] accept neurosurgical intervention as early as 3 months of age; others [9-11], however, are not in favor of early neurosurgical intervention. The objective was to determine the role of some clinical and laboratory approaches in the assessment of the severity of the plexus lesions and to identify patients with a poor prognosis who warrant neurosurgical intervention. In this study, 13 infants were monitored with CBPP using the muscle grading system used in the Hospital for Sick Children (HSC) [6,7] as a clinical assessment method and fast spin-echo magnetic resonance imaging (MRI) and electromyography (EMG) as laboratory tests. Patients and Methods
Introduction Recently, congenital brachial plexus palsy (CBPP) has attracted more interest as neurosurgical interventions have become more effective and incidence (0.5-2 in 1,000 live
From the *Department of Pediatrics; Division of Pediatric Neurology, Istanbul University, Medical Faculty of Istanbul; †Department of Pediatrics; Istanbul University, Institute of Child Health; ‡Department of Neurology; Department of Pediatrics; Division of Pediatric Neurology; and §Department of Radiology; Istanbul University, Medical Faculty of Istanbul; Istanbul, Turkey.
© 1999 by Elsevier Science Inc. All rights reserved. PII S0887-8994(99)00073-9 ● 0887-8994/99/$20.00
The study group encompassed 13 newborns (four females, nine males) with CBPP who had been referred to the authors’ pediatric neurology division. The HSC scoring system (Table 1) was used in the clinical evaluation every 3 months. The patients were monitored until 12 months of age. The brachial plexus and posterior fossa were evaluated with fast spin-echo MRI (Siemens 1.5-T vision, Erlangen, Germany, 512 matrix, head coil) between 7 and 41 days of age (mean ⫽ 21). In T1-weighted
Communications should be addressed to: Dr. C¸alıs¸kan; Istanbul Tıp Faku¨ltesi; C¸ocuk Sag˘lıg˘ı ve Hastalıkları Anabilim Dalı; Gelis¸im No¨rolojisi Bilim Dalı; C¸apa 34390 Istanbul, Tu¨rkiye. Received July 30, 1998; accepted June 15, 1999.
Yılmaz et al: Congenital Brachial Plexus Palsy 705
Table 1.
Hospital for Sick Children muscle grading system Motion
Score
Gravity eliminated No contraction Contraction, no motion Motion ⱕ1⁄2 range Motion ⱖ1⁄2 range Full motion Against gravity Motion ⱕ1⁄2 range Motion ⱖ1⁄2 range Full motion
0 0.3 0.3 0.6 0.6 0.6 1.3 2
scans, the TE (time of echo) was 13-20 ms and the TR (time of repetition) was 600 ms; in T2-weighted scans, the TE was 90-120 ms and the TR was 4,500-7,200 ms. A light sedation was induced with oral chloral hydrate. The imaging was completed in 15-20 minutes. The patients with pathologic MRI findings underwent control scans at 3 months of age. On MRI scans, pseudomeningoceles (PM) were uniform lesions in the signal characteristics of the cerebrospinal fluid and were associated with the ipsilateral neural foramina. The electrophysiologic studies were performed at about 1 month of age (minimum 27 days; maximum 50 days) and 3 months of age. Nerve conduction studies with surface electrodes (sensorial nerves from fingers 1, 3, and 5; motor nerves from the thenar and hypothenar areas; and the musculocutaneous nerve) and needle EMG (abductor digiti minimi, forearm extensors, biceps, triceps, and deltoid muscles) were performed with Medelec MS 92 B (Neurostar) (Medelec, Oxfordshire, UK) equipment. On the basis of each electrophysiologic examination, the functional outcome of the muscles innervated by the upper (C5-C6, upper trunk) and lower (C8-T1, lower trunk) regions of the brachial plexus was determined. A more detailed anatomic categorization could not be made because the number of electrophysiologic studies that can be performed in newborns is limited. Electrophysiologic findings were classified into one of three predictive outcome groups. A poor outcome was indicated by profuse fibrillations and positive waves on needle EMG, with unrecordable or scanty motor unit potentials, no muscle response with the stimulation of motor nerves, and no improvement at the second EMG examination but normal sensory conduction studies, suggesting nerve root avulsion in the presence of severe denervation in the upper extremity muscles. A good outcome was indicated by easily recordable motor unit potentials on needle EMG, absent or rare fibrillations and positive waves, recordable muscle responses with motor nerve stimulation, unrecordable or low-amplitude sensory nerve action potentials, localizing the lesions sites, and considerable improvement between the first and second examination, especially in the number of voluntary motor unit potentials recorded and in the muscle response amplitude recorded in motor nerve conduction studies. A moderate outcome was indicated by electrophysiologic findings that could only be classified in between the two previous groups. Cranial ultrasound was also performed between 7 and 37 days of age (mean ⫽ 17 days).
Results Eight patients (69%) had Erb-Duchenne palsy, and five patients had upper and lower plexus palsy. Six patients (Patients 2, 4, 5, 9, 10, and 11) had torticollis on the same side; one infant (Patient 9) had Horner’s syndrome as well. The mean birth weight was 4,266 gm (S.D. ⫾ 348, range ⫽ 3,750-5,000 gm). The MRI and EMG findings are summarized in Table 2. In the first MRI scans, PM was delineated in four patients.
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Figure 1. Patient 3 (3 months of age). T2-weighted (TE ⫽ 119 ms, TR ⫽ 5,130 ms) axial image. An extradural cyst extending to the right neural foramen in the C6-C7 segment is present.
The PMs were at the level of C5-6 in two (Patients 3 and 10), C6-7 in four (Patients 3, 8, 9, and 10), and C7-T1 in one (Patient 9). A marked PM was also evident in Patient 9 (Figs 1-3). In the follow-up MRI scans at 3 months of age, another PM was observed at the level of C7-T1 in one patient (Patient 8), and in a second (Patient 3) the PM at level C5-6 was not detectable. The PMs of the patients with upper and lower CBPP could be delineated in all planes, even in the first days after birth. However, the PMs of the patients with Erb-Duchenne palsy were smaller. They could be visualized generally in the axial and coronal planes and were more easily visible at 3 months of age. In addition, asymptomatic posterior fossa hematomas were observed in two patients (Patients 5 and 6) who had normal cranial sonographic scans, and additional soft tissue lesions were evident in the first MRI scans of four patients (Patients 2, 5, 9, and 10). The clinical status at 12 months of age is compared with the EMG findings and HSC grading scores in Table 3. EMG implied root avulsion in three of the five patients with a poor prognosis. According to the EMG findings, a complete recovery was predicted in all patients with Erb-Duchenne palsy, all of whom had a favorable prognosis, and poor prognosis was accurately predicted in the patients with upper and lower CBPP, except for one (Patient 7) for whom EMG had indicated a prospect of improvement. The predictions of EMG correlated with the clinical outcome at 12 months of age, except for Patient 7 who had a poor outcome. The predictions of HSC scoring were consistent with the recent clinical condition in all patients. Discussion According to published reports, 80-90% of patients with CBPP have a favorable prognosis (70-80% good, 15-20% mild disability), and about 10-15% have a poor prognosis [9,12]. For most of the patients with favorable prognosis, improvement begins in the first 3 months of age [12];
Table 2.
MRI and EMG findings
Pt. No.
Palsy Level
1
C5-8
Normal (41)
—
Normal
2
C5-6
Normal (38)
—
Normal
3
C5-7
4
C5-8
PMs in right C5-6 PM in right C6-7 Normal (sagittal and (all planes) axial planes) and C6-7 (axial) (8) Normal (22) — Normal
5
C5-6
Normal (7)
—
6
C5-6
Normal (14)
—
7
C5-8
Normal (30)
—
8
C5-8
PM in right C6-7 (all planes) (9)
9
C5-T1 PMs from C3 left Same findings posterolateral to (smaller) T5 anterior and in left C6-C7 and C7-T1 (38) C5-7 PMs in right C6-7 PMs in right C6and possibly 7 and possibly C5-6 (coronal C5-6 (axial plane) (17) and coronal planes) C5-6 N (8) — C5-6 N (32) — C5-6 N (11) —
10
11 12 13
First MRI (age in days)
Second MRI (at 3 mo of age)
Posterior Fossa in First MRI
Associated Findings in First MRI
Findings of First and Second EMG
—
Partial axonal loss in upper plexus, complete in lower; reinnervation in upper plexus in second EMG Mild partial axonal loss in upper plexus; improvement in second EMG Mild partial axonal loss in upper plexus; improvement in second EMG
Edema in right supraspinatus, infraspinatus, teres minor, and subscapularis muscle —
—
Bilateral infratentorial, Bilateral sternocleidomastoid subdural, subacute muscle edema hematomas Right infratentorial, — subdural, subacute hematomas Normal —
PMs in right C6- Normal 7 and C7-T1 (all planes)
—
Normal
Edema in the left rotator cuff and sternocleidomastoid muscle
Normal
Edema in the right rotator cuff
Normal Normal Normal
— — —
Partial axonal loss in upper plexus, complete in lower; reinnervation in upper plexus and root avulsion in lower in second EMG Partial axonal loss in upper plexus
Segmented demyelinization in upper plexus Partial axonal loss in upper plexus, complete in lower; reinnervation in upper plexus Severe axonal loss in upper and lower plexus; reinnervation in upper plexus, root avulsion in lower in second EMG Severe axonal loss in upper and lower plexus; reinnervation in upper plexus, root avulsion in lower in second EMG Severe partial axonal loss in upper plexus; reinnervation in second EMG
Partial axonal loss in upper plexus Partial axonal loss in upper plexus Severe partial axonal loss in upper plexus; reinnervation in second EMG
Abbreviations: EMG ⫽ Electromyography MRI ⫽ Magnetic resonance imaging PM ⫽ Pseudomeningocele
however, in some it is delayed to 4-6 months of age [9,13]. The total duration of the improvement process is usually 12 but sometimes 24 months [14,15]. Currently, the most important problem is to predict the prognosis of the patient as early as possible. In compliance with the reports [6,7,16] that proposed testing several muscles the authors used the HSC system using five motions as evaluation criteria (elbow flexion and elbow, wrist, fingers, and thumb extension) (Table 1) [6,7]. If the total weighted score in the first 3 months of age was higher than 3.5, a
favorable prognosis by 12 months of age was expected with a 94.8% confidence level. In the authors’ study, improvement in most patients with only upper plexus injury began in the first 2 months and reached a satisfactory level by 3 months of age. Only in one patient (Patient 10) was the improvement observed between the third and sixth months. The course of improvement in the authors’ study was in agreement with the previous studies. The total scores of the patients with upper and lower plexus injuries were less than 3.5 in all the physical examinations.
Yılmaz et al: Congenital Brachial Plexus Palsy 707
Figure 2. (A) Patient 8 at 9 days of age. A T2-weighted (TE ⫽ 120 ms, TR ⫽ 5,840 ms) sagittal image. A cystic lesion, isointense compared with cerebrospinal fluid, is present posterior to the seventh cervical vertebral body. (B) Patient 8 at 3 months of age. T2-weighted (TE ⫽ 90 ms, TR ⫽ 4,500 ms) coronal image. A spinal cyst in the posterior (C4-C5) and anterior (C6-T5) of the spinal cord is compressing the spinal cord.
The predictive power of HSC correlated strongly with the outcome in the authors’ study (a sample coefficient of 1). Nevertheless, further studies are required to make a definitive conclusion about its reliability. MRI has been used in the evaluation of brachial plexus lesions of adults for more than 10 years [17,18]. It can delineate the surrounding tissues of the plexus, the plexus intensity, the neuroma, and sometimes even the avulsion lesion itself [19,20]. Moreover, it can be used in many planes, needs a shorter time and light anesthesia, is not invasive, reveals focal spinal lesions, and does not give rise to complications resulting from intrathecal contrast
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Figure 3. Patient 9 (38 days of age). (A) T2-weighted (TE ⫽ 110 ms, TR ⫽ 5,120 ms) sagittal image. A spinal cyst in the posterior (C4-C5) and anterior (C6-T5) of the spinal cord is compressing the spinal cord. (B) T2-weighted (TE ⫽ 110 ms, TR ⫽ 5,120 ms) axial image. In the C6-C7 segment a spinal cyst is evident extending to and causing expansion in the left neural foramina.
administration and radiation. The experience in infants with CBPP are limited in published reports. Miller et al. [21] used MRI (gradient echo sequence) to evaluate the brachial plexus in five infants with a poor prognosis at 3-13 weeks of age. Francel et al. [22] used fast spin-echo MRI (256 matrix) in three infants in the first weeks after birth. The most consistent finding was of PMs, mostly located in the C7 root. The earliest PM was imaged at 6 days of age [22]. Francel et al. [22] emphasized that MRI could be substituted for computed tomography-myelography as a preoperative standard imaging technique, and it
Table 3.
Methods predicting prognosis
Pt. No.
Type Palsy
PM in MRI
Avulsion in EMG
1 2 3 4 5 6 7 8 9 10 11 12 13
Total ED ED Total ED ED Total Total Total ED ED ED ED
No No Yes No No No No Yes Yes Yes No No No
No No No Yes No No No Yes Yes No No No No
EMG Prediction Upper Plexus Lower Plexus Partial Good Good Partial Good Good Partial Partial Poor Good Good Good Good to partial
Poor Normal Normal Poor Normal Normal Good to partial Poor Poor Normal Normal Normal Normal
HSC Scores (3, 6, 9 mo of age)
Prediction of HSC (3 mo of age)
Last Status (12 mo of age)
0, 1.5, 1.8 4.4, 8.6, 10 4.4, 8.6, 10 1.5, 1.5, 1.8 4.4, 9.3, 10 5.6, 10, 10 1.5, 1.5, 1.8 1.5, 1.5, 1.8 1.5, 1.5, 1.8 3.8, 8.6, 9.3 7.9, 10, 10 4.4, 9.3, 10 8.6, 10, 10
Poor Good Good Poor Good Good Poor Poor Poor Good Good Good Good
Poor Good Good Poor Good Good Poor Poor Poor Good Good Good Good
Abbreviations: ED ⫽ Erb-Duchenne EMG ⫽ Electromyography HSC ⫽ Hospital for Sick Children MRI ⫽ Magnetic resonance imaging PM ⫽ Pseudomeningocele
seemed that the PMs were consistent with the prognosis. In the present study the PMs were most commonly observed in the C7 root. The earliest PM was detected at 8 days of age (Patient 3). In one patient (Patient 9) with a poor prognosis a marked PM was observed and may have been an indication of a substantial dural tear. The existence of a PM alone can be an indicator of the severity of the lesion and hence that of the prognosis [21,23]. However, the presence of a PM does not necessarily imply root avulsion. PMs may be visualized even though an avulsion lesion is not present and vice versa [24-26]. In the authors’ study the PMs of the patients with a favorable prognosis were more easily visible in the control scans at 3 months of age than in the scans performed at an earlier age. These findings suggest that PMs that can be delineated in all planes, even in the first days after birth, can be predictive of a poor prognosis. However, this conclusion needs to be corroborated by more data from larger series. The previous studies [21,22] and the present one all demonstrate that MRI can be used in the first days of age with success if needed and that it can substitute for preoperative computed tomographymyelography in infants and in adults. However, using MRI in the first days after birth to predict prognosis is not cost effective, although it may be of predictive value. On the other hand, in the presence of some risk factors (e.g., coexistence of upper and lower plexus palsy, presence of Horner’s syndrome), early MRI evaluation would be reasonable. In this study the patients who had risk factors had a poor prognosis regardless of the existence of PMs on MRI shortly after birth. It should be emphasized that the authors’ study group was too small to conclude that early MRI evaluation is not valuable.
Although the role of EMG in the prediction of the prognosis is still controversial [27-30], EMG can be helpful in locating the lesion (pre- or postganglionic, upper or lower plexus) and determining the severity of the injury. Some technical difficulties in children, such as the appearance of improvement by EMG before the manifestation of clinical signs or limb agnosia (cortical blindness to one’s own arm [6,9]), may all result in misinterpretations. Although EMG overestimated the prognosis in one patient, the EMG findings seemed to help in predicting the outcome. The findings from the authors’ study suggest that if the EMG findings are suspicious for a root avulsion and hence a poor prognosis is expected, EMG is reliable; otherwise, avulsion and a poor prognosis cannot be excluded by EMG only. Moreover, interpretation of EMG findings is subjective and requires some specialization for accurate readings of EMG scans in children. In summary the findings suggest that the most predictive method for prognosis is the HSC muscle grading system. MRI may be the standard imaging technique of the brachial plexus even in the neonatal period. The presence of a PM may be accepted as a sign of root avulsion if interpreted correctly. EMG can be of great value for patients with root avulsion and a poor prognosis but may be relatively too optimistic. In addition, it should be stressed that patients with CBPP should not be monitored with only one criterion. Clinical assessments and laboratory tests should be considered together. In view of these results, infants with CBPP should be monitored with HSC muscle grading, and patients who are expected to have a poor prognosis should be further evaluated with MRI and EMG.
Yılmaz et al: Congenital Brachial Plexus Palsy 709
References [1] Levine MG, Holryode J, Woods Jr JR, et al. Birth trauma: Incidence and predisposing factors. Obstet Gynecol 1984;63:792-5. [2] Jennet RJ, Tarby TJ, Kreinick CJ. Brachial plexus palsy: An old problem revisited. Am J Obstet Gynecol 1992;166:1673-7. [3] Gilbert A, Razaboni R, Amar-Khodja S. Indications and results of brachial plexus surgery in obstetrical palsy. Orthop Clin North Am 1988;19:91-108. [4] Gilbert A, Whitaker I. Obsterical brachial plexus lesions. J Hand Surg [Br] 1991;16:489-91. [5] Laurent JP, Lee R, Shenaq S, Parke JT, Solis IS, Kowalik L. Neurosurgical correction of upper brachial plexus birth injuries. J Neurosurg 1993;79:197-202. [6] Michelow BJ, Clarke HM, Curtis CG, Zuker RM, Seifu Y, Andrews D. The natural history of obstetrical brachial plexus palsy. Plast Recontr Surg 1994;93:675-80. [7] Clarke HM, Curtis CG. An approach to obstetrical brachial plexus injuries. Hand Clin 1995;11:563-80. [8] Gilbert A. Long-term evaluation of brachial plexus surgery in obstetrical palsy. Hand Clin 1995;11:583-94. [9] Eng GD, Binder H, Getson P, O’Donnel R. Obstetrical brachial plexus palsy (OBPP) outcome with conservative management. Muscle Nerve 1996;19:884-91. [10] Kline DG, Hackett ER, Happel LH. Surgery for lesions of the brachial plexus. Arch Neurol 1986;43:170-81. [11] Kay S. Obstetrical brachial palsy. Basis for management. St James’s University Hospital, England. Available at http://www.leeds. ac.uk/handsurgey/obp.htm. Accessed October 2, 1997. [12] Greenwald AG, Schute PC, Shiveley J. Brachial plexus birth palsy: A 10 year report on the incidence and prognosis. J Pediatr Orthop 1984;4:689-92. [13] Carvalho GA, Nikkhah G, Matthies C, Penkert G, Samii M. Diagnosis of root avulsions in traumatic brachial plexus injuries: Value of computerized tomography, myelography and magnetic resonance imaging. Neurosurgery 1997;86:69-76. [14] Brown KLB. Review of obstetrical palsies. Clin Plast Surg 1984;11:181-4. [15] Meyer RD. Treatment of adult and obstetrical brachial plexus injuries. Orthopedics 1986;9:899-903.
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[16] Zancolli EA, Zancolli Jr ER. Palliative surgical procedures in sequelae of obstetric palsy. Hand Clin 1988;4:643-69. [17] Kneeland JB, Kellman GM, Middleton WD, et al. Diagnosis of diseases of the supraclavicular region by use of MR imaging. Am J Roentgenol 1987;148:1149-51. [18] Rapopart S, Blair DN, McCarthy SM, Desser TS, Hammere LW, Sostman HD. Brachial plexus: Correlation of MR imaging with CT and pathological findings. Radiology 1988;167:161-5. [19] Roger B, Travers V, Laval-Jentet M. Imaging of posttraumatic brachial plexus injury. Clin Orthop 1988;237:57-61. [20] Gupta RK, Mehta VS, Banerji AK, Jain RK. MR evaluation of brachial plexus injuries. Neuroradiology 1989;31:377-81. [21] Miller SF, Glasier CM, Griebel ML, Boop F. Brachial plexopathy in infants after traumatic delivery. Evaluation with MR imaging. Radiology 1993;189:481-4. [22] Francel PC, Koby M, Park TS, et al. Fast spin-echo magnetic resonance imaging for radiological assessment of neonatal brachial plexus injury. J Neurosurg 1995;83:461-6. [23] Hashimoto T, Mitomo M, Hirabuki N, et al. Nerve root avulsion of birth palsy: Comparison of myelography with CT myelography and somatosensory evoked potential. Radiology 1991;178:841-45. [24] Taylor PE. Traumatic intradural avulsion of the nerve root of the brachial plexus. Brain 1962;85:579-602. [25] Davies ER, Sutton D, Bligh AS. Myelography in brachial plexus injury. Br J Radiol 1966;39:362-71. [26] Kewalramani LS, Taylor RG. Brachial plexus avulsion: Role of myelography. J Trauma 1975;15:603-8. [27] Smith SJM. The role of neurophysiological investigation in traumatic brachial plexus lesions in adults and children. J Hand Surg 1996;21B:145-7. [28] Jahnke Jr AH, Bovill DF, McCarroll Jr HR, et al. Persistent brachial plexus birth palsies. J Pediatr Orthop 1991;11:533-8. [29] Laurent JP, Lee RT. Birth-related upper brachial plexus injuries in infants. Operative and non-operative approaches. J Child Neurol 1994;9:111-7. [30] Hentz VR, Meyer RD. Brachial plexus microsurgery in children. Microsurgery 1992;12:175-82.
births) has not decreased during the past 20 years [1,2]. Although CBPP has long been recognized as a health problem, prognosis data about CBPP in published reports are not clear enough. Most patients with CBPP improve spontaneously or with physical therapy, although some require additional treatment, such as neurosurgery. However, the best methods to assess the severity of the plexus lesions and to predict candidates for neurosurgical intervention and their outcomes are still controversial. Many clinical and laboratory approaches have been recommended. Gilbert et al. [3,4] proposed improvement in the flexion of the biceps muscle as a criterion of resolution, and Laurent et al. [5] suggested using the biceps, triceps, and deltoid muscles. Michelow et al. [6] and Clarke and Curtis [7] advocated using several other muscles. Some investigators [4,8] accept neurosurgical intervention as early as 3 months of age; others [9-11], however, are not in favor of early neurosurgical intervention. The objective was to determine the role of some clinical and laboratory approaches in the assessment of the severity of the plexus lesions and to identify patients with a poor prognosis who warrant neurosurgical intervention. In this study, 13 infants were monitored with CBPP using the muscle grading system used in the Hospital for Sick Children (HSC) [6,7] as a clinical assessment method and fast spin-echo magnetic resonance imaging (MRI) and electromyography (EMG) as laboratory tests. Patients and Methods
Introduction Recently, congenital brachial plexus palsy (CBPP) has attracted more interest as neurosurgical interventions have become more effective and incidence (0.5-2 in 1,000 live
From the *Department of Pediatrics; Division of Pediatric Neurology, Istanbul University, Medical Faculty of Istanbul; †Department of Pediatrics; Istanbul University, Institute of Child Health; ‡Department of Neurology; Department of Pediatrics; Division of Pediatric Neurology; and §Department of Radiology; Istanbul University, Medical Faculty of Istanbul; Istanbul, Turkey.
© 1999 by Elsevier Science Inc. All rights reserved. PII S0887-8994(99)00073-9 ● 0887-8994/99/$20.00
The study group encompassed 13 newborns (four females, nine males) with CBPP who had been referred to the authors’ pediatric neurology division. The HSC scoring system (Table 1) was used in the clinical evaluation every 3 months. The patients were monitored until 12 months of age. The brachial plexus and posterior fossa were evaluated with fast spin-echo MRI (Siemens 1.5-T vision, Erlangen, Germany, 512 matrix, head coil) between 7 and 41 days of age (mean ⫽ 21). In T1-weighted
Communications should be addressed to: Dr. C¸alıs¸kan; Istanbul Tıp Faku¨ltesi; C¸ocuk Sag˘lıg˘ı ve Hastalıkları Anabilim Dalı; Gelis¸im No¨rolojisi Bilim Dalı; C¸apa 34390 Istanbul, Tu¨rkiye. Received July 30, 1998; accepted June 15, 1999.
Yılmaz et al: Congenital Brachial Plexus Palsy 705
Table 1.
Hospital for Sick Children muscle grading system Motion
Score
Gravity eliminated No contraction Contraction, no motion Motion ⱕ1⁄2 range Motion ⱖ1⁄2 range Full motion Against gravity Motion ⱕ1⁄2 range Motion ⱖ1⁄2 range Full motion
0 0.3 0.3 0.6 0.6 0.6 1.3 2
scans, the TE (time of echo) was 13-20 ms and the TR (time of repetition) was 600 ms; in T2-weighted scans, the TE was 90-120 ms and the TR was 4,500-7,200 ms. A light sedation was induced with oral chloral hydrate. The imaging was completed in 15-20 minutes. The patients with pathologic MRI findings underwent control scans at 3 months of age. On MRI scans, pseudomeningoceles (PM) were uniform lesions in the signal characteristics of the cerebrospinal fluid and were associated with the ipsilateral neural foramina. The electrophysiologic studies were performed at about 1 month of age (minimum 27 days; maximum 50 days) and 3 months of age. Nerve conduction studies with surface electrodes (sensorial nerves from fingers 1, 3, and 5; motor nerves from the thenar and hypothenar areas; and the musculocutaneous nerve) and needle EMG (abductor digiti minimi, forearm extensors, biceps, triceps, and deltoid muscles) were performed with Medelec MS 92 B (Neurostar) (Medelec, Oxfordshire, UK) equipment. On the basis of each electrophysiologic examination, the functional outcome of the muscles innervated by the upper (C5-C6, upper trunk) and lower (C8-T1, lower trunk) regions of the brachial plexus was determined. A more detailed anatomic categorization could not be made because the number of electrophysiologic studies that can be performed in newborns is limited. Electrophysiologic findings were classified into one of three predictive outcome groups. A poor outcome was indicated by profuse fibrillations and positive waves on needle EMG, with unrecordable or scanty motor unit potentials, no muscle response with the stimulation of motor nerves, and no improvement at the second EMG examination but normal sensory conduction studies, suggesting nerve root avulsion in the presence of severe denervation in the upper extremity muscles. A good outcome was indicated by easily recordable motor unit potentials on needle EMG, absent or rare fibrillations and positive waves, recordable muscle responses with motor nerve stimulation, unrecordable or low-amplitude sensory nerve action potentials, localizing the lesions sites, and considerable improvement between the first and second examination, especially in the number of voluntary motor unit potentials recorded and in the muscle response amplitude recorded in motor nerve conduction studies. A moderate outcome was indicated by electrophysiologic findings that could only be classified in between the two previous groups. Cranial ultrasound was also performed between 7 and 37 days of age (mean ⫽ 17 days).
Results Eight patients (69%) had Erb-Duchenne palsy, and five patients had upper and lower plexus palsy. Six patients (Patients 2, 4, 5, 9, 10, and 11) had torticollis on the same side; one infant (Patient 9) had Horner’s syndrome as well. The mean birth weight was 4,266 gm (S.D. ⫾ 348, range ⫽ 3,750-5,000 gm). The MRI and EMG findings are summarized in Table 2. In the first MRI scans, PM was delineated in four patients.
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Figure 1. Patient 3 (3 months of age). T2-weighted (TE ⫽ 119 ms, TR ⫽ 5,130 ms) axial image. An extradural cyst extending to the right neural foramen in the C6-C7 segment is present.
The PMs were at the level of C5-6 in two (Patients 3 and 10), C6-7 in four (Patients 3, 8, 9, and 10), and C7-T1 in one (Patient 9). A marked PM was also evident in Patient 9 (Figs 1-3). In the follow-up MRI scans at 3 months of age, another PM was observed at the level of C7-T1 in one patient (Patient 8), and in a second (Patient 3) the PM at level C5-6 was not detectable. The PMs of the patients with upper and lower CBPP could be delineated in all planes, even in the first days after birth. However, the PMs of the patients with Erb-Duchenne palsy were smaller. They could be visualized generally in the axial and coronal planes and were more easily visible at 3 months of age. In addition, asymptomatic posterior fossa hematomas were observed in two patients (Patients 5 and 6) who had normal cranial sonographic scans, and additional soft tissue lesions were evident in the first MRI scans of four patients (Patients 2, 5, 9, and 10). The clinical status at 12 months of age is compared with the EMG findings and HSC grading scores in Table 3. EMG implied root avulsion in three of the five patients with a poor prognosis. According to the EMG findings, a complete recovery was predicted in all patients with Erb-Duchenne palsy, all of whom had a favorable prognosis, and poor prognosis was accurately predicted in the patients with upper and lower CBPP, except for one (Patient 7) for whom EMG had indicated a prospect of improvement. The predictions of EMG correlated with the clinical outcome at 12 months of age, except for Patient 7 who had a poor outcome. The predictions of HSC scoring were consistent with the recent clinical condition in all patients. Discussion According to published reports, 80-90% of patients with CBPP have a favorable prognosis (70-80% good, 15-20% mild disability), and about 10-15% have a poor prognosis [9,12]. For most of the patients with favorable prognosis, improvement begins in the first 3 months of age [12];
Table 2.
MRI and EMG findings
Pt. No.
Palsy Level
1
C5-8
Normal (41)
—
Normal
2
C5-6
Normal (38)
—
Normal
3
C5-7
4
C5-8
PMs in right C5-6 PM in right C6-7 Normal (sagittal and (all planes) axial planes) and C6-7 (axial) (8) Normal (22) — Normal
5
C5-6
Normal (7)
—
6
C5-6
Normal (14)
—
7
C5-8
Normal (30)
—
8
C5-8
PM in right C6-7 (all planes) (9)
9
C5-T1 PMs from C3 left Same findings posterolateral to (smaller) T5 anterior and in left C6-C7 and C7-T1 (38) C5-7 PMs in right C6-7 PMs in right C6and possibly 7 and possibly C5-6 (coronal C5-6 (axial plane) (17) and coronal planes) C5-6 N (8) — C5-6 N (32) — C5-6 N (11) —
10
11 12 13
First MRI (age in days)
Second MRI (at 3 mo of age)
Posterior Fossa in First MRI
Associated Findings in First MRI
Findings of First and Second EMG
—
Partial axonal loss in upper plexus, complete in lower; reinnervation in upper plexus in second EMG Mild partial axonal loss in upper plexus; improvement in second EMG Mild partial axonal loss in upper plexus; improvement in second EMG
Edema in right supraspinatus, infraspinatus, teres minor, and subscapularis muscle —
—
Bilateral infratentorial, Bilateral sternocleidomastoid subdural, subacute muscle edema hematomas Right infratentorial, — subdural, subacute hematomas Normal —
PMs in right C6- Normal 7 and C7-T1 (all planes)
—
Normal
Edema in the left rotator cuff and sternocleidomastoid muscle
Normal
Edema in the right rotator cuff
Normal Normal Normal
— — —
Partial axonal loss in upper plexus, complete in lower; reinnervation in upper plexus and root avulsion in lower in second EMG Partial axonal loss in upper plexus
Segmented demyelinization in upper plexus Partial axonal loss in upper plexus, complete in lower; reinnervation in upper plexus Severe axonal loss in upper and lower plexus; reinnervation in upper plexus, root avulsion in lower in second EMG Severe axonal loss in upper and lower plexus; reinnervation in upper plexus, root avulsion in lower in second EMG Severe partial axonal loss in upper plexus; reinnervation in second EMG
Partial axonal loss in upper plexus Partial axonal loss in upper plexus Severe partial axonal loss in upper plexus; reinnervation in second EMG
Abbreviations: EMG ⫽ Electromyography MRI ⫽ Magnetic resonance imaging PM ⫽ Pseudomeningocele
however, in some it is delayed to 4-6 months of age [9,13]. The total duration of the improvement process is usually 12 but sometimes 24 months [14,15]. Currently, the most important problem is to predict the prognosis of the patient as early as possible. In compliance with the reports [6,7,16] that proposed testing several muscles the authors used the HSC system using five motions as evaluation criteria (elbow flexion and elbow, wrist, fingers, and thumb extension) (Table 1) [6,7]. If the total weighted score in the first 3 months of age was higher than 3.5, a
favorable prognosis by 12 months of age was expected with a 94.8% confidence level. In the authors’ study, improvement in most patients with only upper plexus injury began in the first 2 months and reached a satisfactory level by 3 months of age. Only in one patient (Patient 10) was the improvement observed between the third and sixth months. The course of improvement in the authors’ study was in agreement with the previous studies. The total scores of the patients with upper and lower plexus injuries were less than 3.5 in all the physical examinations.
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Figure 2. (A) Patient 8 at 9 days of age. A T2-weighted (TE ⫽ 120 ms, TR ⫽ 5,840 ms) sagittal image. A cystic lesion, isointense compared with cerebrospinal fluid, is present posterior to the seventh cervical vertebral body. (B) Patient 8 at 3 months of age. T2-weighted (TE ⫽ 90 ms, TR ⫽ 4,500 ms) coronal image. A spinal cyst in the posterior (C4-C5) and anterior (C6-T5) of the spinal cord is compressing the spinal cord.
The predictive power of HSC correlated strongly with the outcome in the authors’ study (a sample coefficient of 1). Nevertheless, further studies are required to make a definitive conclusion about its reliability. MRI has been used in the evaluation of brachial plexus lesions of adults for more than 10 years [17,18]. It can delineate the surrounding tissues of the plexus, the plexus intensity, the neuroma, and sometimes even the avulsion lesion itself [19,20]. Moreover, it can be used in many planes, needs a shorter time and light anesthesia, is not invasive, reveals focal spinal lesions, and does not give rise to complications resulting from intrathecal contrast
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Figure 3. Patient 9 (38 days of age). (A) T2-weighted (TE ⫽ 110 ms, TR ⫽ 5,120 ms) sagittal image. A spinal cyst in the posterior (C4-C5) and anterior (C6-T5) of the spinal cord is compressing the spinal cord. (B) T2-weighted (TE ⫽ 110 ms, TR ⫽ 5,120 ms) axial image. In the C6-C7 segment a spinal cyst is evident extending to and causing expansion in the left neural foramina.
administration and radiation. The experience in infants with CBPP are limited in published reports. Miller et al. [21] used MRI (gradient echo sequence) to evaluate the brachial plexus in five infants with a poor prognosis at 3-13 weeks of age. Francel et al. [22] used fast spin-echo MRI (256 matrix) in three infants in the first weeks after birth. The most consistent finding was of PMs, mostly located in the C7 root. The earliest PM was imaged at 6 days of age [22]. Francel et al. [22] emphasized that MRI could be substituted for computed tomography-myelography as a preoperative standard imaging technique, and it
Table 3.
Methods predicting prognosis
Pt. No.
Type Palsy
PM in MRI
Avulsion in EMG
1 2 3 4 5 6 7 8 9 10 11 12 13
Total ED ED Total ED ED Total Total Total ED ED ED ED
No No Yes No No No No Yes Yes Yes No No No
No No No Yes No No No Yes Yes No No No No
EMG Prediction Upper Plexus Lower Plexus Partial Good Good Partial Good Good Partial Partial Poor Good Good Good Good to partial
Poor Normal Normal Poor Normal Normal Good to partial Poor Poor Normal Normal Normal Normal
HSC Scores (3, 6, 9 mo of age)
Prediction of HSC (3 mo of age)
Last Status (12 mo of age)
0, 1.5, 1.8 4.4, 8.6, 10 4.4, 8.6, 10 1.5, 1.5, 1.8 4.4, 9.3, 10 5.6, 10, 10 1.5, 1.5, 1.8 1.5, 1.5, 1.8 1.5, 1.5, 1.8 3.8, 8.6, 9.3 7.9, 10, 10 4.4, 9.3, 10 8.6, 10, 10
Poor Good Good Poor Good Good Poor Poor Poor Good Good Good Good
Poor Good Good Poor Good Good Poor Poor Poor Good Good Good Good
Abbreviations: ED ⫽ Erb-Duchenne EMG ⫽ Electromyography HSC ⫽ Hospital for Sick Children MRI ⫽ Magnetic resonance imaging PM ⫽ Pseudomeningocele
seemed that the PMs were consistent with the prognosis. In the present study the PMs were most commonly observed in the C7 root. The earliest PM was detected at 8 days of age (Patient 3). In one patient (Patient 9) with a poor prognosis a marked PM was observed and may have been an indication of a substantial dural tear. The existence of a PM alone can be an indicator of the severity of the lesion and hence that of the prognosis [21,23]. However, the presence of a PM does not necessarily imply root avulsion. PMs may be visualized even though an avulsion lesion is not present and vice versa [24-26]. In the authors’ study the PMs of the patients with a favorable prognosis were more easily visible in the control scans at 3 months of age than in the scans performed at an earlier age. These findings suggest that PMs that can be delineated in all planes, even in the first days after birth, can be predictive of a poor prognosis. However, this conclusion needs to be corroborated by more data from larger series. The previous studies [21,22] and the present one all demonstrate that MRI can be used in the first days of age with success if needed and that it can substitute for preoperative computed tomographymyelography in infants and in adults. However, using MRI in the first days after birth to predict prognosis is not cost effective, although it may be of predictive value. On the other hand, in the presence of some risk factors (e.g., coexistence of upper and lower plexus palsy, presence of Horner’s syndrome), early MRI evaluation would be reasonable. In this study the patients who had risk factors had a poor prognosis regardless of the existence of PMs on MRI shortly after birth. It should be emphasized that the authors’ study group was too small to conclude that early MRI evaluation is not valuable.
Although the role of EMG in the prediction of the prognosis is still controversial [27-30], EMG can be helpful in locating the lesion (pre- or postganglionic, upper or lower plexus) and determining the severity of the injury. Some technical difficulties in children, such as the appearance of improvement by EMG before the manifestation of clinical signs or limb agnosia (cortical blindness to one’s own arm [6,9]), may all result in misinterpretations. Although EMG overestimated the prognosis in one patient, the EMG findings seemed to help in predicting the outcome. The findings from the authors’ study suggest that if the EMG findings are suspicious for a root avulsion and hence a poor prognosis is expected, EMG is reliable; otherwise, avulsion and a poor prognosis cannot be excluded by EMG only. Moreover, interpretation of EMG findings is subjective and requires some specialization for accurate readings of EMG scans in children. In summary the findings suggest that the most predictive method for prognosis is the HSC muscle grading system. MRI may be the standard imaging technique of the brachial plexus even in the neonatal period. The presence of a PM may be accepted as a sign of root avulsion if interpreted correctly. EMG can be of great value for patients with root avulsion and a poor prognosis but may be relatively too optimistic. In addition, it should be stressed that patients with CBPP should not be monitored with only one criterion. Clinical assessments and laboratory tests should be considered together. In view of these results, infants with CBPP should be monitored with HSC muscle grading, and patients who are expected to have a poor prognosis should be further evaluated with MRI and EMG.
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