Childs Nerv Syst (2015) 31:1541–1546 DOI 10.1007/s00381-015-2789-0
ORIGINAL PAPER
Long-term outcome of accessory nerve to suprascapular nerve transfer in obstetric brachial plexus lesion: functional, morphological, and electrophysiological results Matthias Gmeiner 1,3 & Raffi Topakian 2 & Manuel Göschl 4 & Sarah Wurm 1 & Anita Holzinger 4 & Willem J. R. van Ouwerkerk 5 & Kurt Holl 1,3
Received: 7 April 2015 / Accepted: 9 June 2015 / Published online: 26 June 2015 # Springer-Verlag Berlin Heidelberg 2015
Abstract Purpose An accessory to suprascapular nerve (XIN-SSN) transfer is considered in patients with obstetric brachial plexus lesion who fail to recover active shoulder external rotation. The aim of this study was to evaluate the quality of extraplexal suprascapular nerve neurotization and to perform a detailed analysis of the infraspinatus muscle (IM) and shoulder external rotation. Methods A XIN-SSN transfer was performed in 14 patients between 2000 and 2007. Patients had been operated at the age of 3.7±2.8 years. Follow-up examinations were conducted up to 8.5±2.5 years. Magnetic resonance imaging was performed to investigate muscle trophism. Fatty muscle degeneration of the IM was classified according to the Goutallier classification. We conducted nerve conduction velocity studies of the suprascapular nerve and needle electromyography of the IM to assess pathologic spontaneous activity and interference patterns. Active glenohumeral shoulder external rotation and global shoulder function were evaluated using the Mallet score.
* Matthias Gmeiner [email protected] 1
Department of Neurosurgery, Landes-Nervenklinik Wagner-Jauregg, Wagner-Jauregg-Weg 15, A-4020 Linz, Austria
2
Department of Neurology, General Hospital Wels, Wels, Austria
3
Department of Pediatric Neurosurgery, Children’s Hospital, Linz, Austria
4
Department of Radiology, Landes-Nervenklinik Wagner-Jauregg Linz, Linz, Austria
5
Department of Neurosurgery, Vrije Universiteit University Medical Centre Amsterdam, Amsterdam, The Netherlands
Results Postoperatively, growth of the IM increased equally on the affected and unaffected sides, although significant differences of muscle thickness persisted over time. There was only grade 1 or 2 fatty degeneration pre- and postoperatively. Electromyography of the IM revealed a full interference pattern in all except one patient, and there was no pathological spontaneous activity. Glenohumeral external rotation as well as global shoulder function increased significantly. Conclusion Our results indicate that the anastomosis after XIN-SSN transfer is functional and that successful reinnervation of the infraspinatus muscle may enable true glenohumeral active external rotation. Keywords Obstetric brachial plexus lesion . Accessory to suprascapular nerve transfer . Developmental apraxia . Nerve repair
Introduction Obstetric brachial plexus lesion (OBPL) is caused by traction injury during delivery. Although many children show good spontaneous recovery, in 20–30 % of patients, residual deficits are expected [15]. Restoration of shoulder function including active external rotation is a critical goal, but its optimal treatment remains controversial [22]. The infraspinatus muscle (IM) supplied by the suprascapular nerve (SSN) is the primary external rotator of the arm. Further, the supraspinatus, teres minor, deltoid, and triceps brachii muscle are involved in external rotation. Therefore, an accessory nerve to suprascapular nerve (XIN-SSN) transfer is regarded as a primary or secondary treatment option to restore active shoulder external rotation, however, with variable clinical results [22, 14, 17, 20, 8, 7, 3, 21, 18]. As functional improvement may be executed by
1542
thoracoscapular rather than true glenohumeral movement [15], accurate evaluation of SSN neurotization is warranted. In this study, we evaluated the quality of neurotization after XIN-SSN transfer by assessing IM morphology and function using clinical evaluation, electrophysiology, and magnetic resonance imaging (MRI).
Methods This study was approved by the local ethics committee (Ethikkommission des Landes Oberösterreich, EK-Nr. 1656/2012). Fourteen children with OBPL, who failed to recover any external rotation, were treated at the Children’s Hospital in Linz, Austria, between 2000 and 2007. Nine cases of this study were presented recently [22]. Here, we present our single center experience with five additional patients and an extended follow-up. Preoperatively, children received conservative management including an intense program of weekly physiotherapy and daily exercises directed at stimulation of active shoulder external rotation and preserving passive shoulder mobility. In 13 children, the XIN-SSN transfer was finally considered as primary operative treatment. In one child, a complex plexus reconstruction was performed at the age of 4 months. After 1 year, a XIN-SSN and intercostal to musculocutaneous transfer was done as a secondary operative treatment. Intraoperatively, response of infra- and supraspinatus muscle after electrostimulation of the SSN was recorded. Electric stimulation in all exposed SSN provoked motor responses. The SSN was anatomically intact in all patients, and macroscopically, we observed no scarring. Histologic evaluation of the SSN was not performed in this study. If indicated [22], a shoulder release by subscapular tendon lengthening and reposition of the humerus head were performed by an orthopedist simultaneously. All XIN-SSN transfers were performed by the same pediatric neurosurgeon (WJRVO). The XIN was explored from the upper anterior rim of the trapezius muscle using a 3-cm supraclavicular skin incision. Then, the XIN was traced and a branch was cut distally from the muscle, transferred, and neurotized with fibrin glue to the SSN, which was just cut after branching off from the superior trunk [22]. The following patient characteristics were documented: sex (gender), first or later delivery, complications during pregnancy, associated birth lesions, birth weight, previous plexus exploration, patient’s age at surgery, and whether or not a combined shoulder release had been performed. Examinations for this study were performed preoperatively and 8.5 years±2.5 after operation. MRI scans (1.5 T; Verio, TIM; T1, T2, and TSE sequences) were performed to investigate muscle trophism and fatty muscle degeneration of the IM.
Childs Nerv Syst (2015) 31:1541–1546
Fatty muscle degeneration was classified according to the Goutallier classification [6]: grade 0, normal muscle; grade 1, some fatty streaks; grade 2, 50 % fatty muscle atrophy. Nerve conduction velocities (NCV) of the SSN were done by stimulating the nerve at Erb’s point and measuring latency and amplitude of the signal depicted over the IM. Needle electromyography (Keypoint, Medtronic Inc., USA) of the IM was done to assess presence of pathologic spontaneous activity and fullness of interference pattern on maximal voluntary contraction. Preoperatively, none of the patients had any active external rotation. For postoperative evaluation, we set the maximal endorotation to zero and then evaluated external rotation (Fig. 1). To avoid trick movements, the upper arm was gently held in adduction by the investigator and the elbow was actively flexed in 90° [15]. Shoulder function was additionally evaluated using the modified Mallet scale for abduction, external rotation, and hand-to-mouth movement adapted from Aydin et al. (Fig. 2 [1]). Statistical analyses were performed using the Shapiro-Wilk test, Wilcoxon signed-rank test, and the t test for paired samples. All analyses were performed by SPSS for Windows (SPSS, Inc. Chicago, IL). Data are expressed as mean±standard deviation, and the statistical significance level is set at p2nd Birth weight 4 kg Delivery Spontaneous Instrumental Pregnancy complications Associated birth lesions (y/n) Age at operation XIN-SSN 24 months Shoulder release combined (y/n)
10/4
2 12 4 10 8 6 2 7/7 7 7 5/9
XIN accessory nerve, SSN suprascapular nerve, y yes, n no, m male, f female
Muscle thickness and fatty degeneration The muscle thickness of the IM on the affected side increased by 58.8 % from 6.8 mm± 1.4 preoperatively to 10.8 mm±2.2 postoperatively (n=11). Muscle thickness on the unaffected side increased by 56.1 % from 9.5 mm±0.9 to 14.8 mm ±2.1. These data clearly demonstrate that muscle growth rate was comparable on both sides (58.8 versus 56.1 %). Muscle thickness of the affected arm was significantly smaller pre- and postoperatively as compared to the healthy arm. Fatty muscle degeneration according to the Goutallier classification showed grade 0 in four patients and grade 1 in seven patients before XIN-SSN transfer versus grade 0 in three patients and grade 1 in eight patients after surgery. These data indicate that the degree of fatty degeneration remains stable after operation.
Electrophysiology NCV measurements (n=11) of the SSN revealed a mean latency of 2.83 ms (±1) and a mean amplitude of 5.14 mV (±2.5). Needle electromyography (n=11) of the IM on the affected side did not reveal pathologic spontaneous activity. Analysis of motor unit potentials showed signs of chronic neurogenic changes with relatively high amplitudes (median 1.60 mV, range 0.39–1.80 mV) but normal polyphasia rate (median 10 %, range 8.3–10 %). Interference pattern during maximal voluntary contraction was semiquantitatively subdivided into full, slightly reduced, or markedly reduced: We found a full interference pattern in 10 patients and a slightly reduced interference pattern in one patient.
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Childs Nerv Syst (2015) 31:1541–1546 Table 3 Mallet score for abduction, external rotation and hand-tomouth movement
External rotation Preoperatively, none of the patients was able to exorotate. For this analysis, we set the maximal endorotation to zero and then evaluated external rotation (n=14). External rotation improved in 12 patients and increased to 88.2°±47 (range 45– 155). In only two patients, there was no improvement. Functional level was defined as 95° external rotation and was achieved in nine patients (65 %) (Fig. 1, Table 2). Mallet score The Mallet score for abduction, external rotation, and hand-tomouth is illustrated in Table 3, Fig. 2 (n=14). A significant improvement was achieved in external rotation and hand-tomouth (p
ORIGINAL PAPER
Long-term outcome of accessory nerve to suprascapular nerve transfer in obstetric brachial plexus lesion: functional, morphological, and electrophysiological results Matthias Gmeiner 1,3 & Raffi Topakian 2 & Manuel Göschl 4 & Sarah Wurm 1 & Anita Holzinger 4 & Willem J. R. van Ouwerkerk 5 & Kurt Holl 1,3
Received: 7 April 2015 / Accepted: 9 June 2015 / Published online: 26 June 2015 # Springer-Verlag Berlin Heidelberg 2015
Abstract Purpose An accessory to suprascapular nerve (XIN-SSN) transfer is considered in patients with obstetric brachial plexus lesion who fail to recover active shoulder external rotation. The aim of this study was to evaluate the quality of extraplexal suprascapular nerve neurotization and to perform a detailed analysis of the infraspinatus muscle (IM) and shoulder external rotation. Methods A XIN-SSN transfer was performed in 14 patients between 2000 and 2007. Patients had been operated at the age of 3.7±2.8 years. Follow-up examinations were conducted up to 8.5±2.5 years. Magnetic resonance imaging was performed to investigate muscle trophism. Fatty muscle degeneration of the IM was classified according to the Goutallier classification. We conducted nerve conduction velocity studies of the suprascapular nerve and needle electromyography of the IM to assess pathologic spontaneous activity and interference patterns. Active glenohumeral shoulder external rotation and global shoulder function were evaluated using the Mallet score.
* Matthias Gmeiner [email protected] 1
Department of Neurosurgery, Landes-Nervenklinik Wagner-Jauregg, Wagner-Jauregg-Weg 15, A-4020 Linz, Austria
2
Department of Neurology, General Hospital Wels, Wels, Austria
3
Department of Pediatric Neurosurgery, Children’s Hospital, Linz, Austria
4
Department of Radiology, Landes-Nervenklinik Wagner-Jauregg Linz, Linz, Austria
5
Department of Neurosurgery, Vrije Universiteit University Medical Centre Amsterdam, Amsterdam, The Netherlands
Results Postoperatively, growth of the IM increased equally on the affected and unaffected sides, although significant differences of muscle thickness persisted over time. There was only grade 1 or 2 fatty degeneration pre- and postoperatively. Electromyography of the IM revealed a full interference pattern in all except one patient, and there was no pathological spontaneous activity. Glenohumeral external rotation as well as global shoulder function increased significantly. Conclusion Our results indicate that the anastomosis after XIN-SSN transfer is functional and that successful reinnervation of the infraspinatus muscle may enable true glenohumeral active external rotation. Keywords Obstetric brachial plexus lesion . Accessory to suprascapular nerve transfer . Developmental apraxia . Nerve repair
Introduction Obstetric brachial plexus lesion (OBPL) is caused by traction injury during delivery. Although many children show good spontaneous recovery, in 20–30 % of patients, residual deficits are expected [15]. Restoration of shoulder function including active external rotation is a critical goal, but its optimal treatment remains controversial [22]. The infraspinatus muscle (IM) supplied by the suprascapular nerve (SSN) is the primary external rotator of the arm. Further, the supraspinatus, teres minor, deltoid, and triceps brachii muscle are involved in external rotation. Therefore, an accessory nerve to suprascapular nerve (XIN-SSN) transfer is regarded as a primary or secondary treatment option to restore active shoulder external rotation, however, with variable clinical results [22, 14, 17, 20, 8, 7, 3, 21, 18]. As functional improvement may be executed by
1542
thoracoscapular rather than true glenohumeral movement [15], accurate evaluation of SSN neurotization is warranted. In this study, we evaluated the quality of neurotization after XIN-SSN transfer by assessing IM morphology and function using clinical evaluation, electrophysiology, and magnetic resonance imaging (MRI).
Methods This study was approved by the local ethics committee (Ethikkommission des Landes Oberösterreich, EK-Nr. 1656/2012). Fourteen children with OBPL, who failed to recover any external rotation, were treated at the Children’s Hospital in Linz, Austria, between 2000 and 2007. Nine cases of this study were presented recently [22]. Here, we present our single center experience with five additional patients and an extended follow-up. Preoperatively, children received conservative management including an intense program of weekly physiotherapy and daily exercises directed at stimulation of active shoulder external rotation and preserving passive shoulder mobility. In 13 children, the XIN-SSN transfer was finally considered as primary operative treatment. In one child, a complex plexus reconstruction was performed at the age of 4 months. After 1 year, a XIN-SSN and intercostal to musculocutaneous transfer was done as a secondary operative treatment. Intraoperatively, response of infra- and supraspinatus muscle after electrostimulation of the SSN was recorded. Electric stimulation in all exposed SSN provoked motor responses. The SSN was anatomically intact in all patients, and macroscopically, we observed no scarring. Histologic evaluation of the SSN was not performed in this study. If indicated [22], a shoulder release by subscapular tendon lengthening and reposition of the humerus head were performed by an orthopedist simultaneously. All XIN-SSN transfers were performed by the same pediatric neurosurgeon (WJRVO). The XIN was explored from the upper anterior rim of the trapezius muscle using a 3-cm supraclavicular skin incision. Then, the XIN was traced and a branch was cut distally from the muscle, transferred, and neurotized with fibrin glue to the SSN, which was just cut after branching off from the superior trunk [22]. The following patient characteristics were documented: sex (gender), first or later delivery, complications during pregnancy, associated birth lesions, birth weight, previous plexus exploration, patient’s age at surgery, and whether or not a combined shoulder release had been performed. Examinations for this study were performed preoperatively and 8.5 years±2.5 after operation. MRI scans (1.5 T; Verio, TIM; T1, T2, and TSE sequences) were performed to investigate muscle trophism and fatty muscle degeneration of the IM.
Childs Nerv Syst (2015) 31:1541–1546
Fatty muscle degeneration was classified according to the Goutallier classification [6]: grade 0, normal muscle; grade 1, some fatty streaks; grade 2, 50 % fatty muscle atrophy. Nerve conduction velocities (NCV) of the SSN were done by stimulating the nerve at Erb’s point and measuring latency and amplitude of the signal depicted over the IM. Needle electromyography (Keypoint, Medtronic Inc., USA) of the IM was done to assess presence of pathologic spontaneous activity and fullness of interference pattern on maximal voluntary contraction. Preoperatively, none of the patients had any active external rotation. For postoperative evaluation, we set the maximal endorotation to zero and then evaluated external rotation (Fig. 1). To avoid trick movements, the upper arm was gently held in adduction by the investigator and the elbow was actively flexed in 90° [15]. Shoulder function was additionally evaluated using the modified Mallet scale for abduction, external rotation, and hand-to-mouth movement adapted from Aydin et al. (Fig. 2 [1]). Statistical analyses were performed using the Shapiro-Wilk test, Wilcoxon signed-rank test, and the t test for paired samples. All analyses were performed by SPSS for Windows (SPSS, Inc. Chicago, IL). Data are expressed as mean±standard deviation, and the statistical significance level is set at p2nd Birth weight 4 kg Delivery Spontaneous Instrumental Pregnancy complications Associated birth lesions (y/n) Age at operation XIN-SSN 24 months Shoulder release combined (y/n)
10/4
2 12 4 10 8 6 2 7/7 7 7 5/9
XIN accessory nerve, SSN suprascapular nerve, y yes, n no, m male, f female
Muscle thickness and fatty degeneration The muscle thickness of the IM on the affected side increased by 58.8 % from 6.8 mm± 1.4 preoperatively to 10.8 mm±2.2 postoperatively (n=11). Muscle thickness on the unaffected side increased by 56.1 % from 9.5 mm±0.9 to 14.8 mm ±2.1. These data clearly demonstrate that muscle growth rate was comparable on both sides (58.8 versus 56.1 %). Muscle thickness of the affected arm was significantly smaller pre- and postoperatively as compared to the healthy arm. Fatty muscle degeneration according to the Goutallier classification showed grade 0 in four patients and grade 1 in seven patients before XIN-SSN transfer versus grade 0 in three patients and grade 1 in eight patients after surgery. These data indicate that the degree of fatty degeneration remains stable after operation.
Electrophysiology NCV measurements (n=11) of the SSN revealed a mean latency of 2.83 ms (±1) and a mean amplitude of 5.14 mV (±2.5). Needle electromyography (n=11) of the IM on the affected side did not reveal pathologic spontaneous activity. Analysis of motor unit potentials showed signs of chronic neurogenic changes with relatively high amplitudes (median 1.60 mV, range 0.39–1.80 mV) but normal polyphasia rate (median 10 %, range 8.3–10 %). Interference pattern during maximal voluntary contraction was semiquantitatively subdivided into full, slightly reduced, or markedly reduced: We found a full interference pattern in 10 patients and a slightly reduced interference pattern in one patient.
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Childs Nerv Syst (2015) 31:1541–1546 Table 3 Mallet score for abduction, external rotation and hand-tomouth movement
External rotation Preoperatively, none of the patients was able to exorotate. For this analysis, we set the maximal endorotation to zero and then evaluated external rotation (n=14). External rotation improved in 12 patients and increased to 88.2°±47 (range 45– 155). In only two patients, there was no improvement. Functional level was defined as 95° external rotation and was achieved in nine patients (65 %) (Fig. 1, Table 2). Mallet score The Mallet score for abduction, external rotation, and hand-tomouth is illustrated in Table 3, Fig. 2 (n=14). A significant improvement was achieved in external rotation and hand-tomouth (p
