COMPARISON OF OBJECTIVE MUSCLE STRENGTH IN C5-C6 AND C5-C7 BRACHIAL PLEXUS INJURY PATIENTS AFTER DOUBLE NERVE TRANSFER YI-JUNG TSAI, P.T., M.SC.,1 FONG-CHIN SU, Ph.D.,1,2 CHIH-KUN HSIAO, Ph.D.,3 and YUAN-KUN TU, M.D.1,4*
Purpose: The purpose of this study was to evaluate the quantitative muscle strength to distinguish the outcomes of different injury levels in upper arm type brachial plexus injury (BPI) patients with double nerve transfer. Methods: Nine patients with C5-C6 lesions (age 5 32.2 6 13.9 year old) and nine patients with C5-C7 lesions (age 5 32.4 6 7.9 year old) received neurotization of the spinal accessory nerve to the suprascapular nerve combined with the Oberlin procedure (fascicles of ulnar nerve transfer to the musculocutaneous nerve) were recruited. The average time interval between operation and evaluation were 27.3 6 21.0 and 26.9 6 20.6 months for C5-C6 and C5-C7, respectively. British Medical Research Council (BMRC) scores and the objective strength measured by a handheld dynamometer were evaluated in multiple muscles to compare outcomes between C5-C6 and C5-C7 injuries. Results: There were no significant differences in BMRC scores between the groups. C5-C6 BPI patients had greater quantitative strength in shoulder flexor (P 5 0.02), shoulder extensor (P < 0.01), elbow flexor (P 5 0.04), elbow extensor (P 5 0.04), wrist extensor (P 5 0.04), and hand grip (P 5 0.04) than C5-C7 BPI patients. Conclusions: Upper arm type BPI patients have a good motor recovery after double nerve transfer. The different outcomes between C5-C6 and C5-C7 BPI patients appeared in muscles responding to hand grip, wrist extension, and sagittal movements in C 2014 Wiley Periodicals, Inc. Microsurgery 35:107–114, 2015. shoulder and elbow joints. V
Traumatic brachial plexus injuries (BPI) usually occur in young male adults, and are mostly caused by a highenergy force such as motorcycle accidents.1,2 According to the injury level, traumatic BPI are commonly classified into upper (C5-C6 or C5-C7 lesions), total (C5-T1 total avulsion), and lower (C8-T1 lesions) types.3 The functional activities of daily life are limited due to deficiencies in motor and sensory function of innervated muscles following such injuries. For BPI patients, obtaining the shoulder functions in elevation, abduction, external rotation, and elbow flexion are often set as the primary goals of reconstruction. Neurotization is one of the procedures for shoulder and elbow reconstruction, and good outcomes of various donor nerves have been reported.4–11 The spinal accessory nerve (SAN) transfer to the suprascapular nerve (SSN) is the prevailing procedures for shoulder reconstruction,4,6,10 while the Oberlin procedure, which involves transferring fascicles of the
1 Department of Biomedical Engineering, National Cheng Kung University, Tainan, Taiwan, Republic of China 2 Medical Device Innovation Center, National Cheng Kung University, Tainan, Taiwan, Republic of China 3 Department of Medical Research, E-Da Hospital, Kaohsiung, Taiwan, Republic of China 4 Department of Orthopedics, E-Da Hospital, Kaohsiung, Taiwan, Republic of China Grant sponsor: National Science Council of Taiwan; grant number: 100– 2221-E-650-002. *Correspondence to: Yuan-Kun Tu, M.D., Department of Orthopedics, E-Da Hospital, No. 1, Yida Road, Jiaosu Village, Yanchao District, Kaohsiung, Taiwan, Republic of China. E-mail: [email protected] Received 26 March 2014; Revised 15 May 2014; Accepted 21 May 2014 Published online 17 June 2014 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/micr.22283
Ó 2014 Wiley Periodicals, Inc.
ulnar nerve (UN) to the musculocutaneous nerve (MCN), is used commonly for elbow function repair.9 The injury level is critical to determine the reconstruction procedure and outcome.5,11–15 Favorable results have been reported in upper type BPI after nerve transfer, but the outcomes of patients with C5-C6 or C5-C7 lesions are often discussed together.16–18 Furthermore, few studies have investigated the recovery of multiple joints simultaneously. Therefore, the purposes of this study were to evaluate the quantitative muscle strength in C5-C6 and C5-C7 BPI patients after double nerve transfer (SAN to SSN and UN to MCN), and distinguish the outcomes between different injury levels. PATIENTS AND METHODS
We conducted a prospective study to evaluate the outcomes of double nerve transfer. Patients diagnosed with upper trunk lesions of the brachial plexus and underwent neurotization procedures from 2006 to 2011 were recruited. The injury level was confirmed by electromyography (EMG), nerve conduction velocity (NCV), and intraoperative findings. All patients had paralysis in shoulder flexion and elbow flexion before operation. In C5-C6 BPI, the wrist and finger dorsiflexion of injured upper limbs were preserved. While in C5-C7 BPI, patients were observed to have poor wrist and finger (metacarpal-phalangeal joint) dorsiflexion of injured limbs (M0–M1). All subjects received nerve transfer of the SAN to SSN and UN to MCN by an experienced surgeon at the Department of Orthopedics of E-Da Hospital in Taiwan. The surgical indications for double nerve transfer in this study were as followings: (1) Upper arm type BPI
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diagnosis confirmed by EMG, NCV, and clinical neurological examination; (2) C5-C6 or C5-C7 roots avulsion were confirmed by preoperative magnetic resonance imaging and intra-operative findings; (3) C5-C6 or C5C7 nerve cutting injury which could not be repaired by primary nerve suture, such as iatrogenic thermal or cutting injury during neck surgery; (4) The associated injuries, such as the skeletal fracture, head injury or abdominal trauma had been adequately treated with stable physical recovery; and (5) The interval between the injury and surgical intervention must be within 1 year. Subjects were excluded if they had stab or sharp cut injury of brachial plexus (surgery performed by primary nerve repair), severe deformities, joint contracture, cardiovascular disorders, or other problems that would affect the evaluation. This study was approved by the Institutional Review Board of E-Da Hospital, and written informed consent was obtained from each participant before the examination. Nine patients (1 female, 8 males) with C5-C6 injuries and 9 patients (1 female, 8 males) with C5-C7 injuries were recruited. Information including age, body weight (BW), body height, injury side, causation, and dominant hand before/after injury were recorded. British Medical Research Council (BMRC) Score Evaluation
The motor recovery was first evaluated by the BMRC scoring system conducted in a sitting position.19 Muscle groups including shoulder flexor, extensor, abductor, external rotator, internal rotator, elbow flexor, extensor, and wrist extensor were evaluated. A score less than M3 was defined as a poor result, with M0 defined as no contraction, M1 observable contraction, and M2 active movement with gravity eliminated. The patients were asked to keep their trunk erect to prevent compensatory movements during the examination. The examiner stabilized the proximal region and provided the necessary support. Quantitative Strength Measurement
Quantitative muscle strength was measured with a handheld dynamometer (HHD; MicroFET2, Hoggan Health Industries). All measurements were conducted in the supine position for better stability of the trunk and scapular regions, and to prevent unnecessary movements during force generation.20 The limb position, placement of the HHD, and placement of stabilization were as previously reported.21,22 One or two practice trials with a submaximal force were performed to make sure the patients understood how to push against the dynamometer correctly. Muscles of both upper extremities were examined by a well-trained physiotherapist. The subjects were asked to exert maximum isometric strength against Microsurgery DOI 10.1002/micr
the dynamometer, and the noninvolved arm was tested first. Each muscle was measured two times, and 30second and 1-minute resting intervals were provided between repeated trials and different muscle groups, respectively. Grip strength was measured by the Jamar Plus1 Digital Hand Dynamometer (Sammons Preston). The test was performed in a sitting position with elbow flexion at 90 . The examiner stabilized the wrist during test, and patients were encouraged to exert the grip force as much as possible. Both arms were measured two times, and a 30-second resting interval between trials. Statistical Analysis
The average of two trials for all muscle groups and grip strength was calculated for further analysis. The quantitative values were normalized to the BW. Independent t-tests and chi-square tests were used to compare the differences between the groups. Statistical analysis was performed with SPSS version 17.0 (SPSS, Chicago, IL), and a P value 0.05; Table 2). Quantitative Strength
The normalized quantitative strength and ratio between involved and noninvolved arms are demonstrated in Table 3. There were no complaints about discomfort during the evaluation with the HHD. No significant difference was found in the strength of the noninvolved arm between the two groups (P > 0.05). In the involved arm, the strength in the C5-C6 group
Quantitative Strength of Upper Arm BPI Table 1. Comparisons of Demographic Data in the C5-C6 and C5-C7 BPI Patients C5-C6 (n 5 9)
C5-C7 (n 5 9)
8/1 4/5
8/1 4/5
7 2 0 32.2 6 13.9 171.9 6 8.7 71.8 6 8.1 27.3 6 21.0
6 1 2 32.4 6 7.9 170.5 6 7.9 73.9 6 11.5 26.9 6 20.6
Gender (male/female) Injury side (left/right) Causation Traffic accident (motorcycle) Cut injurya Fall Age (years) Body height (cm) BW (kg) Follow-up duration (months) a
Cut injury: iatrogenic injury during neck surgery.
showed a trend of being greater than that in the C5-C7 group, ranging from 4.0 6 2.9% BW (shoulder external rotator) to 17.3 6 5.7% BW (shoulder extensor) in the C5-C6 group, and 3.0 6 1.8% BW (shoulder external rotator) to 9.0 6 6.1% BW (shoulder abductor) in the C5C7 group. The strength ratio between both arms showed that the patients with C5-C6 lesions had restoration of nearly or more than half the strength of the noninvolved arm in shoulder flexor (49.8 6 29.1%), extensor (64.8 6 23.5%), abductor (44.7623.0%), elbow extensor (57.5628.2%), Table 2. BMRC Grade of Each Muscle in Both Groups No. of Patients (%)
Purpose: The purpose of this study was to evaluate the quantitative muscle strength to distinguish the outcomes of different injury levels in upper arm type brachial plexus injury (BPI) patients with double nerve transfer. Methods: Nine patients with C5-C6 lesions (age 5 32.2 6 13.9 year old) and nine patients with C5-C7 lesions (age 5 32.4 6 7.9 year old) received neurotization of the spinal accessory nerve to the suprascapular nerve combined with the Oberlin procedure (fascicles of ulnar nerve transfer to the musculocutaneous nerve) were recruited. The average time interval between operation and evaluation were 27.3 6 21.0 and 26.9 6 20.6 months for C5-C6 and C5-C7, respectively. British Medical Research Council (BMRC) scores and the objective strength measured by a handheld dynamometer were evaluated in multiple muscles to compare outcomes between C5-C6 and C5-C7 injuries. Results: There were no significant differences in BMRC scores between the groups. C5-C6 BPI patients had greater quantitative strength in shoulder flexor (P 5 0.02), shoulder extensor (P < 0.01), elbow flexor (P 5 0.04), elbow extensor (P 5 0.04), wrist extensor (P 5 0.04), and hand grip (P 5 0.04) than C5-C7 BPI patients. Conclusions: Upper arm type BPI patients have a good motor recovery after double nerve transfer. The different outcomes between C5-C6 and C5-C7 BPI patients appeared in muscles responding to hand grip, wrist extension, and sagittal movements in C 2014 Wiley Periodicals, Inc. Microsurgery 35:107–114, 2015. shoulder and elbow joints. V
Traumatic brachial plexus injuries (BPI) usually occur in young male adults, and are mostly caused by a highenergy force such as motorcycle accidents.1,2 According to the injury level, traumatic BPI are commonly classified into upper (C5-C6 or C5-C7 lesions), total (C5-T1 total avulsion), and lower (C8-T1 lesions) types.3 The functional activities of daily life are limited due to deficiencies in motor and sensory function of innervated muscles following such injuries. For BPI patients, obtaining the shoulder functions in elevation, abduction, external rotation, and elbow flexion are often set as the primary goals of reconstruction. Neurotization is one of the procedures for shoulder and elbow reconstruction, and good outcomes of various donor nerves have been reported.4–11 The spinal accessory nerve (SAN) transfer to the suprascapular nerve (SSN) is the prevailing procedures for shoulder reconstruction,4,6,10 while the Oberlin procedure, which involves transferring fascicles of the
1 Department of Biomedical Engineering, National Cheng Kung University, Tainan, Taiwan, Republic of China 2 Medical Device Innovation Center, National Cheng Kung University, Tainan, Taiwan, Republic of China 3 Department of Medical Research, E-Da Hospital, Kaohsiung, Taiwan, Republic of China 4 Department of Orthopedics, E-Da Hospital, Kaohsiung, Taiwan, Republic of China Grant sponsor: National Science Council of Taiwan; grant number: 100– 2221-E-650-002. *Correspondence to: Yuan-Kun Tu, M.D., Department of Orthopedics, E-Da Hospital, No. 1, Yida Road, Jiaosu Village, Yanchao District, Kaohsiung, Taiwan, Republic of China. E-mail: [email protected] Received 26 March 2014; Revised 15 May 2014; Accepted 21 May 2014 Published online 17 June 2014 in Wiley Online Library (wileyonlinelibrary.com). DOI: 10.1002/micr.22283
Ó 2014 Wiley Periodicals, Inc.
ulnar nerve (UN) to the musculocutaneous nerve (MCN), is used commonly for elbow function repair.9 The injury level is critical to determine the reconstruction procedure and outcome.5,11–15 Favorable results have been reported in upper type BPI after nerve transfer, but the outcomes of patients with C5-C6 or C5-C7 lesions are often discussed together.16–18 Furthermore, few studies have investigated the recovery of multiple joints simultaneously. Therefore, the purposes of this study were to evaluate the quantitative muscle strength in C5-C6 and C5-C7 BPI patients after double nerve transfer (SAN to SSN and UN to MCN), and distinguish the outcomes between different injury levels. PATIENTS AND METHODS
We conducted a prospective study to evaluate the outcomes of double nerve transfer. Patients diagnosed with upper trunk lesions of the brachial plexus and underwent neurotization procedures from 2006 to 2011 were recruited. The injury level was confirmed by electromyography (EMG), nerve conduction velocity (NCV), and intraoperative findings. All patients had paralysis in shoulder flexion and elbow flexion before operation. In C5-C6 BPI, the wrist and finger dorsiflexion of injured upper limbs were preserved. While in C5-C7 BPI, patients were observed to have poor wrist and finger (metacarpal-phalangeal joint) dorsiflexion of injured limbs (M0–M1). All subjects received nerve transfer of the SAN to SSN and UN to MCN by an experienced surgeon at the Department of Orthopedics of E-Da Hospital in Taiwan. The surgical indications for double nerve transfer in this study were as followings: (1) Upper arm type BPI
108
Tsai et al.
diagnosis confirmed by EMG, NCV, and clinical neurological examination; (2) C5-C6 or C5-C7 roots avulsion were confirmed by preoperative magnetic resonance imaging and intra-operative findings; (3) C5-C6 or C5C7 nerve cutting injury which could not be repaired by primary nerve suture, such as iatrogenic thermal or cutting injury during neck surgery; (4) The associated injuries, such as the skeletal fracture, head injury or abdominal trauma had been adequately treated with stable physical recovery; and (5) The interval between the injury and surgical intervention must be within 1 year. Subjects were excluded if they had stab or sharp cut injury of brachial plexus (surgery performed by primary nerve repair), severe deformities, joint contracture, cardiovascular disorders, or other problems that would affect the evaluation. This study was approved by the Institutional Review Board of E-Da Hospital, and written informed consent was obtained from each participant before the examination. Nine patients (1 female, 8 males) with C5-C6 injuries and 9 patients (1 female, 8 males) with C5-C7 injuries were recruited. Information including age, body weight (BW), body height, injury side, causation, and dominant hand before/after injury were recorded. British Medical Research Council (BMRC) Score Evaluation
The motor recovery was first evaluated by the BMRC scoring system conducted in a sitting position.19 Muscle groups including shoulder flexor, extensor, abductor, external rotator, internal rotator, elbow flexor, extensor, and wrist extensor were evaluated. A score less than M3 was defined as a poor result, with M0 defined as no contraction, M1 observable contraction, and M2 active movement with gravity eliminated. The patients were asked to keep their trunk erect to prevent compensatory movements during the examination. The examiner stabilized the proximal region and provided the necessary support. Quantitative Strength Measurement
Quantitative muscle strength was measured with a handheld dynamometer (HHD; MicroFET2, Hoggan Health Industries). All measurements were conducted in the supine position for better stability of the trunk and scapular regions, and to prevent unnecessary movements during force generation.20 The limb position, placement of the HHD, and placement of stabilization were as previously reported.21,22 One or two practice trials with a submaximal force were performed to make sure the patients understood how to push against the dynamometer correctly. Muscles of both upper extremities were examined by a well-trained physiotherapist. The subjects were asked to exert maximum isometric strength against Microsurgery DOI 10.1002/micr
the dynamometer, and the noninvolved arm was tested first. Each muscle was measured two times, and 30second and 1-minute resting intervals were provided between repeated trials and different muscle groups, respectively. Grip strength was measured by the Jamar Plus1 Digital Hand Dynamometer (Sammons Preston). The test was performed in a sitting position with elbow flexion at 90 . The examiner stabilized the wrist during test, and patients were encouraged to exert the grip force as much as possible. Both arms were measured two times, and a 30-second resting interval between trials. Statistical Analysis
The average of two trials for all muscle groups and grip strength was calculated for further analysis. The quantitative values were normalized to the BW. Independent t-tests and chi-square tests were used to compare the differences between the groups. Statistical analysis was performed with SPSS version 17.0 (SPSS, Chicago, IL), and a P value 0.05; Table 2). Quantitative Strength
The normalized quantitative strength and ratio between involved and noninvolved arms are demonstrated in Table 3. There were no complaints about discomfort during the evaluation with the HHD. No significant difference was found in the strength of the noninvolved arm between the two groups (P > 0.05). In the involved arm, the strength in the C5-C6 group
Quantitative Strength of Upper Arm BPI Table 1. Comparisons of Demographic Data in the C5-C6 and C5-C7 BPI Patients C5-C6 (n 5 9)
C5-C7 (n 5 9)
8/1 4/5
8/1 4/5
7 2 0 32.2 6 13.9 171.9 6 8.7 71.8 6 8.1 27.3 6 21.0
6 1 2 32.4 6 7.9 170.5 6 7.9 73.9 6 11.5 26.9 6 20.6
Gender (male/female) Injury side (left/right) Causation Traffic accident (motorcycle) Cut injurya Fall Age (years) Body height (cm) BW (kg) Follow-up duration (months) a
Cut injury: iatrogenic injury during neck surgery.
showed a trend of being greater than that in the C5-C7 group, ranging from 4.0 6 2.9% BW (shoulder external rotator) to 17.3 6 5.7% BW (shoulder extensor) in the C5-C6 group, and 3.0 6 1.8% BW (shoulder external rotator) to 9.0 6 6.1% BW (shoulder abductor) in the C5C7 group. The strength ratio between both arms showed that the patients with C5-C6 lesions had restoration of nearly or more than half the strength of the noninvolved arm in shoulder flexor (49.8 6 29.1%), extensor (64.8 6 23.5%), abductor (44.7623.0%), elbow extensor (57.5628.2%), Table 2. BMRC Grade of Each Muscle in Both Groups No. of Patients (%)
