- Email: [email protected]
Secondary shoulder reconstruction in patients with brachial plexus injuries
Journal of Plastic, Reconstructive & Aesthetic Surgery (2011) 64, 843e853
Secondary shoulder reconstruction in patients with brachial plexus injuries* Julia K. Terzis a,*, Antonia Barmpitsioti b a
Department of Surgery, Division of Plastic and Reconstructive Surgery, Eastern Virginia Medical School (EVMS), 700 Olney Road, LH 2055, Norfolk, VA 23507, USA b Microsurgery Program, Department of Surgery, Eastern Virginia Medical School (EVMS), Norfolk, VA, USA Received 21 May 2010; accepted 28 December 2010
KEYWORDS Brachial plexus; Secondary shoulder reconstruction; Shoulder abduction; Free muscles transfers; Trapezius advancement; External rotation; Latissimus dorsi-teres major rerouting
Summary Restoration of shoulder stability in post-traumatic plexopathy patients is very important because more distal functions depend on a stable and functioning shoulder. The purpose of this study is to present our experience with secondary surgeries in patients with devastating paralysis. Functional outcomes were analyzed in relation to age, severity score and type of reconstruction. The medical records of 55 post-traumatic plexopathy patients who underwent secondary shoulder reconstruction, by a single surgeon, between 1978 and 2006, were reviewed. 55 patients had 73 procedures, 44 for shoulder abduction and 29 for external rotation. 38 patients underwent secondary surgery to augment shoulder abduction. Trapezius advancement was performed in 14 patients, double free muscle transfer in18, free latissimus dorsi in 4 and triceps muscle transfer in 2 patients. 26 patients had secondary procedures for enhancement of shoulder external rotation. Dynamic rerouting of latissimus dorsi and teres major was carried out in 18 patients and rotational humerus osteotomy in 11 patients. All patients had improvement of shoulder stability and function. Shoulder abduction reached 40.80 15.93 and external rotation at 24.28 17.90 . Trapezius advancement yielded 41.81 9.02 of abduction. Latissimus dorsi yielded stronger shoulder abduction than adductor longus. Rerouting of latissimus dorsi and teres major attained 22.33 20.31 of dynamic external rotation while humerus osteotomy produced 26.87 10.32 of external rotation. Secondary procedures such as pedicle and free muscles transfers, tendon transfers, and rotational humerus osteotomy augment shoulder stability and function in patients with irreparable paralysis. ª 2011 British Association of Plastic, Reconstructive and Aesthetic Surgeons. Published by Elsevier Ltd. All rights reserved.
* Informed consent was obtained from each patient. This study was reviewed and approved by the Eastern Virginia Medical School Institutional Review Board. * Corresponding author. E-mail address: [email protected] (J.K. Terzis).
1748-6815/$ - see front matter ª 2011 British Association of Plastic, Reconstructive and Aesthetic Surgeons. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.bjps.2010.12.015
844
J.K. Terzis, A. Barmpitsioti
Introduction
Table 2 Demographic data of 55 post-traumatic plexopathy patients.
Upper extremity palsy due to brachial plexus injuries have been described from antiquity. Surgical attempts to restore function in the injured upper extremity began early in the 20th century.1,2 Over the last 40 years a greater understanding of anatomy and pathophysiology of nerve regeneration, along with the introduction of microsurgery, allowed the development of strategies of reconstruction for brachial plexus injuries with feasible and predictable results.1e5 The shoulder is a complex of joints and muscles that connects the arm to the trunk. Its range of motion is performed by the coordinated movement of the glenohumeral, scapulothoracic, acromioclavicular and sternoclavicular joints which is called the scapulohumeral rhythm. For shoulder abduction-elevation approximately a 2:1 ratio of glenohumeral to scapulothoracic motion is required; 120 of abduction occurs at the glenohumeral joint and 60 at the scapulothoracic joint; the first 30 of abduction occurs mainly at the glenohumeral joint. The deltoid and supraspinatus muscles are the real abductors, while the infraspinatus, posterior deltoid and teres minor function as external rotators.6,7 Shoulder stabilization is very important as more distal motions such as elbow and hand require a stable shoulder for useful function. Lesions of the axillary and suprascapular nerves incapacitate shoulder abduction and external rotation. Primary nerve repair remains the “gold standard” in upper limb reconstruction.8e11 If surgery is early and successful, adequate reinnervation of deltoid, teres minor, supraspinatus and infraspinatus as well as glenohumeral joint stability can be achieved.10,11 Yet, when nerve repair is unsuccessful, or when the interval between injury and surgery is too long, secondary surgeries such as muscle and tendon transfers are needed to improve shoulder function and reduce shoulder subluxation.12e14 In the current study the senior authors’ experience with secondary shoulder reconstruction is presented. Functional outcomes were analyzed in relation to age, severity score and type of reconstruction.
Data
No of patients
Sex
Female: 8 Male: 47 Left: 32 Right: 22 Clavicle: 13 Scapula: 5 Ribs: 5 Axillary: 5 Subclavian: 5 Brachial: 1 25.49 8.66 8.18 5.83 (range 0e22) Normal plexus: 25 Global avulsion: 0 24.18 39.58 months 4.51 2.98
Patients and methods Between 1978 and 2006, a total of 55 patients with posttraumatic brachial plexus palsy underwent secondary shoulder reconstruction in our Center. The cause of the brachial plexus lesions in 49 patients was motor vehicle accidents (Table 1). The mean age was 25.49 8.66 years. Twenty two (22) patients had associated fractures (reconstruction took place elsewhere) and 11 had vascular injury. The demographic data is shown in Table 2. Table 1 Type of accident for 55 Post-traumatic Brachial Plexus Patients. Type of accident
No. of patients (%)
Motorcycle accident Motor vehicle accident Pedestrian Work related injury
31 (56.3%) 18 (32.7%) 3 (5.45%) 3 (5.45%)
Side Fractures
Vascular injury
Age (years) Severity score
Denervation time Follow-up (years)
Electrodiagnostic evaluation was performed in all patients while relevant angiography was carried out in patients scheduled for free muscle transfers. Meticulous clinical examination was performed in the entire upper extremity using a modified British Medical Research Council Grading System, expanded further with intermediate grades of þ and (e, g., M0 to M2 indicated poor result; M2þ to M3 was a fair result; M3þ to M4 indicated good result; and M4 to M5 was an excellent result).15 The values were recorded on a plexus chart. The passive and active range of shoulder motion was measured; shoulder abduction was measured against gravity starting with the arm at the side; shoulder external rotation was evaluated starting with the arm in the neutral position; the gained degrees of external rotation were measured and recorded. Additionally, preoperative and postoperative behavioral video analysis was carried out by three independent evaluators who viewed standardized videos separately and graded the results. The senior author (J. K. T.) introduced in 1984 a quantitative intraoperative scoring system that provides diagnosis of the brachial plexus lesion at the level of each root (Avulsion Z 0, Avulsion/Rupture Z 1, Rupture Z 2, Traction/Rupture Z 3, Traction Z 4, Normal Z 5). The total Table 3 Type of lesion for each root in 55 Post-traumatic Brachial Plexus Patients. Type of lesion
C5
C6
C7
C8
T1
Total
Avulsion Rupture/Avulsion Rupture Rupture/Traction Traction Normal
5 2 36 1 5 1
21 2 21 2 4 0
36 0 5 1 6 2
30 3 1 1 3 12
23 1 2 1 7 16
115 8 65 6 25 31
36 patients (65.45%) had severity score less than 10. Each root that has not been injured has a score of 5. The normal plexus has 25 severity score. The lower the severity score the worse the injury. There were 5 patients with infraclavicular lesions (9.09%).
Secondary shoulder reconstruction in patients with brachial plexus injuries Table 4
845
Donor nerve used for free muscles reinnervation.
Donor/Recipient
ACC
Cervical plexus
LD ADDL(SH) GRAC(EL)
6 3
4 6
C5
DRS
ICN
cLP
3 3 1
4
cC7
Other
1 4 3
1 1
Acc: Spinal accessory nerve; C5: C5 root; DRS: Dorsal scapular nerve; INC: Intercostal nerves; cLP: Contralateral Lateral Pectoral nerve; cC7: Contralateral C7 root; Other: Medial cord; LD, Latissimus dorsi; ADDL, Adductor longus; GRAC, Gracilis; SH, Shoulder; EL, Elbow.
Table 5
Type of secondary reconstruction in 55 patients with post-traumatic brachial plexus injuries.
Type of reconstruction
DFM
LD
Trap
Tric
PMJ- MI
cTrap
LD-TM
OS
No of patients
18
4
14
2
5
1
18
11
DFM: Double free muscles; LD: free latissimus dorsi; Trap: trapezius advancement; Tric: triceps; LD-TM: Rerouting of latissimus dorsiteres major; TM: teres major; PMJ- MI: pectoralis major- minor; OS: osteotomy; cTrap: contralateral trapezius. A combination of procedures such as free muscle and trapezius or pectoralis advancement took place in 6 patients while latissimus dorsi rerouting and humerus osteotomy was performed in 3 patients.
severity score for a normal plexus is 2515. The lower the severity score the worse the injury. The mean severity score in this series was 8.18 5.83 which reflects the severity of lesions in this patient population. There were 36 patients with severity score less than 10. A total of 115 root avulsions were encountered (Table 3). Primary reconstruction had been performed in 41 patients with axillary and/or suprascapular nerve repair; the resulting function was deemed not satisfactory and further procedures were needed to center the humerus into the glenoid and improve shoulder range of motion. In the current study, 55 patients had 73 procedures, 44 for shoulder abduction and 29 for external rotation. A total of 38 patients underwent reconstruction for restoration of shoulder abduction; in 14 patients the trapezius muscle was advanced for improvement of shoulder abduction; four patients had free contralateral latissimus dorsi transfer and 18 patients had double free muscle transfers, gracilis and adductor longus, for restoring simultaneously shoulder abduction and elbow flexion; the donor nerves for free muscle reinnervation are shown in Table 4. Secondary procedures for augmentation of shoulder external rotation were carried out in 26 patients; dynamic latissimus dorsi and teres major rerouting was
Figure 1 Intraoperative view of the free double muscle transfer prior to insetting.
performed in 18 patients. Rotational humerus osteotomy was performed in 11 patients (Table 5). 9 patients had secondary shoulder reconstruction to augment both abduction and external rotation and 9 patients had more than one procedure for strengthening shoulder stability and function, such as free muscle and trapezius or pectoralis minor advancement (n Z 6), latissimus dorsi rerouting and humerus osteotomy (n Z 3).
Surgical technique Adductor longus and gracilis transfer (Double Free Muscle Transfer) The senior author in 1983 introduced the double free muscle technique for both shoulder abduction and elbow flexion reanimation16. The gracilis was utilized for elbow flexion and the adductor longus for shoulder abduction. This transfer is based on their common vascular pedicle. The muscles were harvested through a curvilinear incision in the medial aspect of the thigh. The skin flaps are developed and the fascia incised to expose both muscles. The pedicle is identified as it enters the undersurface of the gracilis muscle but in this transfer the supplying branches to the adductor longus are preserved. Exploration of this common vascular pedicle leads to the profunda femoris vessels where the common pedicle will be taken. The obturator nerve is identified as it enters the gracilis muscle and intraoperative stimulation secures its integrity. This is traced proximally towards the inguinal ligament and the nerve to the adductor is encountered anterolaterally underneath the adductor longus. Once the neurovascular bundle is exposed both muscles are skeletonized. The common vascular pedicle is short while a respectable length of the supplying nerves 5e7cm can be taken. The muscles prior to transfer are tagged every one centimeter to mark the insitu tension. A second surgical team prepares the pocket in the paralyzed upper extremity where the double muscle unit is to be transferred. The difficulty with this procedure is that upon transfer, the adductor longus is placed laterally and the gracilis medially (see Figure 1). This places the common vascular
846
J.K. Terzis, A. Barmpitsioti
Figure 2 21 year old male was involved in a motor cycle accident. He sustained multiple injuries that lead to exploratory laparotomy, splenectomy, and trachiostomy. He also sustained pneumothorax, fracture of the left scapula, celebral contusion and left brachial plexus injury. 18 months later, the patient presented to our Center with impairment of shoulder abduction (Figure 2a). Exploration of plexus was carried out and microneurolysis of the entire plexus performed. Additionally banked nerves were placed from contralateral lateral pectoral (cLP), C2 and C3 motors and spinal accessory nerve. In another stage a double free muscle was transferred for simultaneous augmentation of elbow extension (gracilis) and shoulder abduction (adductor longus). Neurotisation was done by the cervical motors, C2, and C3 nerves. The patient 4 years later demonstrated 90 of shoulder abduction (Figure 2b).
Figure 3 Intraoperative photo of the contralateral free latissimus transfer prior to insetting.
pedicle laterally about 10e12 cm inferior to the acromion over the middle deltoid. As there are no recipient vessels at that site, long vein grafts are needed for the revascularization of the double muscle unit. The appropriate recipient vessels need to be prepared for end- to- side anastomoses prior to muscle transfer. Recipient vessels include the common carotid or the subclavian artery, and recipient veins include the subclavian, jugular or basilic veins. Insetting of the double muscle free flap is as follows: the gracilis is anchored to the lateral clavicle and the adductor longus to the acromion and spine of the scapula. Distally the gracilis is inserted in the distal biceps tendon, and the adductor longus on the lateral humerus on the deltoid groove and secured in place with compression screws. The original tension of the transplanted muscle units is restored by insetting the muscles with the insitu tension which was marked prior to transfer. Donor motor nerves for reinnervation of the double muscles included: distal spinal accessory,
Figure 4 31 year old male sustained an injury while motorcycle racing. He fell off his motorcycle and struck a wall with tires. He experienced loss of consciousness, right lung contusion, right fifth metacarpal fracture, and right brachial plexus palsy. He was referred to our Center 3 months later with a paralyzed right upper extremity (Figure 4a). Brachial plexus exploration revealed C5 rupture, C6-C7 avulsion and C8-T1 traction. The first stage of reconstruction included: Direct neurotisation of distal spinal accessory to suprascapular nerve, and C4 motor nerve and C5 root to posterior cord with interposition nerve grafts. In the second stage T8, T9 and T10 intercostal nerves neurotized directly the musculocutaneous nerve, T6 and T7 intercostals the long thoracic and T3-T4 intercostals the thoracodorsal nerve; T5 was used as banked nerve. 14 months later the right latissimus dorsi was transferred to augment elbow flexion and the right trapezius was transferred to augment shoulder abduction; humerus rotational osteotomy was also done to increase external rotation, and Steindler flexoplasty to augment elbow flexion. Wrist fusion and tendon transfers were performed 2 years later. The patient after the trapezius transfer presented with 80 of shoulder abduction (Figure 4b).
Secondary shoulder reconstruction in patients with brachial plexus injuries
847
Table 6 Results after secondary shoulder reconstruction (means SD) in 45 evaluated patients with post-traumatic brachial plexus palsy. Total patients with secondary shoulder reconstruction
Shoulder abduction degrees (means SD)
Shoulder external rotation degrees (means SD)
Pre-operative Post-operative Patients after primary reconstruction Pre-operative Post-operative
14.67 12.71 40.80 15.93
8 10.05 24.28 17.90
15.22 12.86 40 17.66
10.71 10.71 26.66 20.14
*The results (preoperative versus postoperative) were statistical significant for all groups (ManneWhitney test, p < 0. 001).
Table 7
Evaluated Functional outcomes versus different motor donor nerves used for free muscle reinnervation.
Donors (number of patients)
Free muscle grading (median, minimumemaximum)
Degrees of shoulder abduction (means SD)
Accessory (n Z 5) Cervical plexus (n Z 4) Intercostal (n Z 2) Dorsal scapular (n Z 3) Contralateral lateral pectoral (n Z 3)
2.33(1.66e3.33) 2.66 (1.33e3.33) 2.33 2.00 (1.33e3.00) 2.33 (1.33e2.33)
9 16.25 5 16.66 6.66
Preop
postop
13.41 12.50 7.07 15.27 11.54
40 15.41 38.33 5.77 30 35 21.79 26.66 5.77
Preop: preoperative; postop: postoperative. Difference between the donors was not statistically significant (KruskaleWallis test, p > 0.05).
Figure 5 Muscle grading versus different motor donor nerves used for free muscle reinnervation (means SD). A: spinal accessory nerve; B: cervical plexus motor donors; C: intercostal nerves; D: dorsal scapular nerve; E: (cLP)contralateral lateral pectoral nerve. Differences between motor donors were not statistically significant (KruskaleWallis test, p > 0.05).
cervical plexus motors, and contralateral lateral pectoral (cLP), (Table 4), (Figures 1 and 2). Latissimus dorsi The latissimus dorsi is harvested through a curved 20 cm incision starting at the axilla and running obliquely toward the posterior iliac spine. The origin of the muscle is
attached proximally along the nuchal line and the spinous processes of the cervical and upper thoracic spine. The distal tendon is secured on the lateral humerus on the deltoid groove. Compression screws are used for solid insetting. Transferring the latissimus dorsi, may on occasion result in webbing in the neck. Correction of this problem was by creation of a pulley, using fascia lata, which is secured on the spinous processes posteriorly to the clavicle anteriorly. The vascular pedicle is long and reaches the axillary or brachial artery. End- to- side anastomoses are performed. The donor nerves included direct intercostal neurotization (3 cases) and one case with the posterior division (PD) of contralateral C7 (cC7), (Table 4), (Figure 3). Trapezius advancement The trapezius is harvested through a curved supraclavicular incision. The lateral clavicular, acromial and spinous insertions of the trapezius are severed and the muscle is mobilized proximally and cranially. The transposed muscle is anchored with two screws in the deltoid insertion on the humerus. Usually, the trapezius needs to be elongated using a strip of fascia lata (Figure 4).
Table 8 Results after different types of reconstruction for shoulder abduction in 45 evaluated patients with post-traumatic brachial plexus palsy. Shoulder function/ Type of reconstunction
Muscle grading (median, minimum-maximum)
Shoulder abduction degrees (means SD) preop
postop
Double free muscles Free Latissimus dorsi Trapezius Advancement
2.33 (1.33e3.33) 2.33 (2.33e3.33) 2.66 (1.33e3.33)
14.33 13.34 3.33 5.77 16.81 12.70
36 13.12 41.66 20.88 41.81 9.02
Preop: preoperative; postop: postoperative. Difference between the types of reconstruction was not statistically significant (KruskaleWallis test p > 0.05).
848
J.K. Terzis, A. Barmpitsioti Postoperative, after free muscle transfer, intensive monitoring for 3 days can prevent postoperative vascular problems. Thus early diagnosis and immediate return to surgery will salvage the free muscle. The upper limb is immobilized in a prefabricated splint for 8 weeks with the arm in 90 abduction and elbow flexion. The splint is gradually adjusted to 60 and then 30 abduction and removed at three months. At six weeks following surgery the patients are fitted with a slow-pulse stimulator which they use five to six times a day. This stimulation protocol is continued until reinnervation takes place.
Statistical analysis
Figure 6 Diagrammatic depiction of the latissimus dorsi and teres major rerouting procedure for dynamic external rotation restoration.
The statistical analysis was performed with the assistance of the Department of Biostatistics of Eastern Virginia Medical School and using the Instat version 3.00 (GraphPad Software, SanDiego, Calif.). The results are presented as means SD and the muscle grading as median (minimum-maximum). Comparison of results was carried out using the ManneWhitney U test and between more than two groups using the KruskalWallis test. P values <0.05 were considered to be significant.
Figure 7 30 year old male sustained a high velocity motorcycle accident, in a collision with a truck. He was wearing a helmet. He experienced loss of consciousness, closed head injury, fracture of the left femur, fracture of the left wrist and fifth metacarpal and a global left brachial plexus palsy. He had previous brachial plexus exploration and reconstruction in another center and had some return of shoulder abduction but no external rotation. He was referred to our center 5 years after the accident (Figure 7a). The intraoperative findings were: rupture of C5, C6, and T1 and avulsion of C7 and C8. Reconstruction in our Center included: T5-T6 to thoracodorsal nerve; T7-T8 to triceps nerve; 75% of the proximal long thoracic to triceps nerve via a short graft; The phrenic nerve (one third), and 75% of the dorsal root of C5 to deep saphenous graft as banked nerve for finger flexors; and the distal accessory to left sural for finger extensors; T5-T6-T7 (sensory) were transferred to the median nerve for restoration of protective sensation to the hand. Furthermore release of pectoralis major and conjoin tendon (right shoulder arthroplasty) was performed followed by rerouting of the right latissimus dorsi and teres major for restoration of shoulder external rotation along with left wrist fusion. One year later, T3, T4, T9, T10 intercostal nerves were used as banked nerves and the left free gracilis was transferred for finger flexion; eight months later, the right gracilis was transferred for finger extension. 3 years later the patient demonstrated excellent shoulder function (fig. 7b) and almost full shoulder external rotation (Figure 7c).
Secondary shoulder reconstruction in patients with brachial plexus injuries
849
Figure 8 24 year old male was involved in a motorcycle accident. He fell on a car exiting a small road because the car violated a stop sign and he hit the side of the car with his body. He experienced unconsciousness and he sustained: right mandibular, left clavicle, left scapula, right thumb fractures; partial dislocation of T7-T8 vertebrae with paraplegia, left subclavian artery injury and left brachial plexus palsy. 23 months following the accident he was referred to our Center with upper plexus palsy (Figure 8a). Plexus exploration revealed C5 and C6 roots traction. The reconstruction at that time included: microneurolysis of C5, C6 roots, upper truck, and suprascapular nerve; A small segment of C5 was used to reconstruct the axillary with the use of interposition nerve grafts; to augment shoulder external rotation rerouting of latissimus dorsi and teres major was carried out. 4 years later the patient had excellent shoulder external rotation (Figure 8b).
Results 41 patients had previously primary nerve reconstruction with inadequate results. Functional outcomes were analyzed in 45 patients who had at least 2 years of followup; the mean follow-up was 4.51 2.98 years. Postoperative evaluation took place at 6 and 12 month intervals. All patients achieved a stable shoulder and in all patients the range of motion was improved (Table 6). Patients with ages less than 20 years obtained superior shoulder abduction (41.45 17.47 ) than older patients (36.66 9.85 ), (ManneWhitney test, p < 0.8); the difference was not statistically significant. Patients with severity score higher than ten regained significant better shoulder abduction (46.66 22.77 ) than patients with severity score less than ten, who regained 38.40 10.95 of abduction (ManneWhitney, p < 0.04). Evaluation of muscle transfers to reinforce shoulder abduction demonstrated that free latissimus dorsi transfer yielded stronger shoulder abduction (median 2.33(2.33e3.33), and 41.66 20.2 of abduction), than adductor longus as double free muscle transfer, which yielded median: 2.33(1.33e3.33) and 36 13.12 of abduction; this difference was not statistically significant (ManneWhitney, p < 0.52). The results from different motor donors are presented in Table 7 and Figure 5. Trapezius muscle advancement achieved median muscle grading 2.66(1.33e3.33), and 41.81 9.02 of shoulder abduction; trapezius muscle, before its advancement, had median grading 4.66, and the shoulder had full passive range of motion (Table 8). To assess the results of external rotation, the difference between the preoperative presentation of the patient, during which the arm was hold in internal rotation and the degrees of external rotation achieved postoperative were recorded; patients with latissimus dorsi and teres major rerouting attained a mean of 22.33 20.31 of external rotation (Figures 6,7 and 8). Humerus rotational osteotomy
yielded a mean of 26.87 10.32 of external rotation (Figures 9,10 and 11). Dynamic shoulder abduction and external rotation was also graded by three independent reviewers who reviewed separately preoperative and postoperative standardized videos of each patient. A total of 99 estimations were carried out for shoulder abduction and 45 for external rotation. There were 51.51% of estimations with more than 30 of abduction, and 46.66% of estimations with more than 15 of external rotation (Figure 12).
Discussion Rajiv17 noticed that brachial plexus injuries affect more than 1% of multitrauma victims; motor cycle injuries comprise 4.2% of brachial plexus damages while 0.67 of motor vehicle victims suffered brachial plexus injuries. The high impact of motor cycle accident can be explained by the increased forces applied to the neck area.1 In our series 75% of patients were involved in high velocity motor vehicle accidents.
Figure 9 Functional results for shoulder external rotation (degrees, means SD) by different types of reconstruction preoperative and postoperative. Differences were statistically significant for both procedures (ManneWhitney test p < 0.003). LD-TM: Latissimus and teres major rerouting procedure.
850
J.K. Terzis, A. Barmpitsioti
Figure 10 This 26 year old male was involved in a motorcycle accident. He was un-helmeted while he struck a bus door with his right side. He sustained the following: loss of consciousness, laceration of the right neck, closed head injury, lung contusion, paralysis of right hemidiaphragm, right tibial fracture, four ribs fracture, and right brachial plexus palsy. 4 months later he underwent brachial plexus exploration overseas. He was referred to our Center 12 months after the accident. His right shoulder was internally rotated and the forearm was held in pronation (Figure 10a). The intraoperative findings were: C5, C6, C7, C8 roots avulsion, T1 root traction. The reconstruction included: Direct neurotisation of the distal accessory nerve to suprascapular; T8, T9 intercostal nerves to axillary nerve; T6, T7, T10 intercostal nerves to musculocutaneous nerve; cC7 root posterior division (PD) via sural nerve grafts to triceps. Secondary reconstruction took place one year later involving tendon transfers for hand reanimation and humerus rotational osteotomy to improve shoulder external rotation. A final stage of reconstruction, 18 months later, involved a trapezius muscle transfer to augment shoulder abduction and wrist fusion. The patient seen at 6 years after the accident demonstrated reversal of the pronation deformity of his right arm (Figure 10b), and good external rotation (Figure 10c).
In Upper Brachial plexus lesions, primary repair of the axillary and suprascapular nerves is the treatment of choice yielding superior results especially in younger patients and when the interval between injury and surgery is short.9e11 Secondary procedures are carried out in cases of delayed presentation and when functional outcomes after primary reconstruction are inadequate.12e14 In this series, 41 patients underwent augmentation of primary reconstruction and all patients had prolonged denervation time (24.18 39.58 months) and multiple root avulsions (8.18 5.83 severity score). Secondary reconstructive strategies depend on the type of the brachial plexus lesion, the availability of local muscles,
good passive shoulder mobility, and at least M4 muscle grading as the transferable muscles always lose one muscle grade upon transfer. Procedures using a variety of muscles have been described.1214 The trapezius muscle transfer has been used since the early 20th century to augment shoulder stability.1820 Mayer19 transferred the trapezius for paralyzed abductors in six patients with gratifying results in four patients. Milessi21 reported that control of shoulder function can be achieved by transferring the trapezius with its bony insertion at the acromion onto the humerus. In Ruhmann’s22 series 82.6% of patients who experienced trapezius transfer expressed their satisfaction from the achieved shoulder stability and
Secondary shoulder reconstruction in patients with brachial plexus injuries
851
Figure 11 This is a 50 year old male who was involved in a high velocity vehicular accident. He was driving the truck; his left arm hit a metal bar. He experienced lost of consciousness and respiratory arrest. He furthermore sustained open wound trauma on the left shoulder and the left chest; fracture of the left ribs, open fracture of the left humerus, and fracture of the left radius, and ulnar; dislocation of the sternoclavicular joint; brachial artery injury; laceration of the face; and left brachial plexus palsy. 8 and ½ months later he presented to our center with a paralyzed left arm internally rotated (Figure 11a). The intraoperative findings included: traction of the left brachial plexus and rupture of the axillary and radial nerves. Extensive microneurolysis was performed as well as reconstruction of axillary and radial nerves. 9 months later the ipsilateral latissimus was transferred as a pedicle flap for elbow flexion, wrist fusion was performed, and bone graft was placed in the humerus fracture area. 2 and ½ years later 30 rotational osteotomy of the humerus was carried out to improve external rotation along with tendon transfers to improve hand function. The patient in a late follow-up (ten years later) demonstrated the gained external rotation and the good position of his upper extremity (Figure 11b).
function. Although Singh18 reported that performing trapezius transfer, patients regained a mean of 116 of shoulder abduction, most authors that used this transfer reported that the improvement of shoulder abduction ranged from 39 to
Figure 12 Preoperative and postoperative dynamic video evaluation for shoulder abduction and external rotation (degrees, means SD); assessment was carried out by three independent investigators. Preoperative the mean shoulder abduction and external rotation was 9.07 18.08 and 11.70 25.30 respectively, and postoperative the shoulder abduction was 39.64 37.14 and external rotation was 26.70 29.72 . Differences were statistically significant (ManneWhitney test, p < 0.006).
60 2225. In our series trapezius transfer yielded a mean of 41.81 9.02 of shoulder abduction. L’Episcopo26 in 1930 described the use of teres major and latissimus dorsi to restore shoulder external rotation in obstetric brachial plexus paralysis (OBPP). Modifications of this procedure have also been reported27,28. Good passive external rotation is a requirement. This procedure is wellestablished in OBPP patients.29,30 Beaucamp31 performed L’Episcopo procedure in 11 adult plexopathy patients and achieved a mean of 28 of external rotation. In the experience of the senior author, the rerouting of latissimus tendon around the humerus yields much better results in children than in adults.30 In this series, the adult patients who underwent this surgery achieved 22.33 20.31 of shoulder external rotation. Where there is a paucity of local muscles for dynamic external rotation restoration, humerus rotational ostetomy is recommended for posture correction32,33. Ruhmann32 using osteotomy in 9 patients with brachial plexus palsy reported 42 of external rotation as well as better upper extremity placement. In the present series the patients who had humerus osteotomy regained a mean of 26.87 10.32 of external rotation, with improvement in upper limb position and appearance. In the 1970’s, a lot of the principles of free muscle transfer were elucidated, which allowed the transfer of a healthy
852 normal muscle to a paralyzed extremity to become a viable reconstructive option.34 The selection of donor muscle depends on the type of blood supply, the length, volume, shape of muscle, architecture of muscles fiber, and force of contraction.35 To restore shoulder abduction by free muscle transfer remains one of the most challenging procedures in reconstructive surgery; the majority of authors use free muscle, mainly to enhance elbow and hand function3537. According to Chuang,37 functional free muscle transplantation for restoration of shoulder function was ineffective because of its complexity; he reported 4 patients where he performed free gracilis transfer to replace the deltoid or supraspinatus muscles and achieved only 20 of shoulder abduction. Itoh38 described a pedicle latissimus transfer to replace the anterior deltoid in 10 patients and in six patients achieved 90 of anterior flexion. Hussl39 used pedicle latissimus dorsi to improve the shoulder’s shape and appearance. The senior author introduced in 1983 the double free muscle transfer-gracilis and adductor longus- for simultaneous shoulder and elbow reconstruction, based on their common vascular pedicle. It is a difficult procedure as long interposition vein grafts are needed for revascularization, and there is a large discrepancy (5e1) in the vessel diameter between vein graft and vascular pedicle. Nevertheless, with one operation two functions can be restored. In our center this procedure was used from 1983 to 1992. Subsequently because of greater demands as far as muscle power in the Caucasian patient, larger muscles were used, and gracilis was used mainly for hand reanimation. Free latissimus transfer achieved stronger glenohumeral joint abduction but occasionally neck webbing occurred. The use of fascia lata as pulley provided a solution.1,3,16 One advantage of the procedure is that one can still use trapezius advancement in patients who need more powerful abduction. In this series, patients with free latissimus transfer regained a mean of 41.66 20.2 of abduction. Shoulder arthrodesis was recommended in the past as a well-recognized procedure to restore shoulder stability in patients with devastating paralysis.2,5,13,14,40 The senior author (J. K. T.), does not advocate glenohumeral joint fusion, because of its high complication rate and pain sequelae; on the contrary she advocates primary reconstruction of the brachial plexus, which if done in a timely manner, will restore useful shoulder stability and function.1,3 In late cases, free muscle transfers provide better function, less complications and can be combined with other procedures (like trapezius advancement) to further strengthen shoulder abduction.
Conclusion Restoration of shoulder stability is very important in patients with brachial plexopathies prior to pursuing reanimation of the forearm and hand. Secondary procedures can provide shoulder stabilization and improved function when results after primary reconstruction are inadequate or in late cases with long denervation time. Trapezius advancement and/or free muscle transfers can augment shoulder abduction and improve shoulder stability. Rerouting of latissimus and teres major can restore some dynamic external rotation. If local muscles are not available, rotational osteotomy of the
J.K. Terzis, A. Barmpitsioti humerus can place the paretic upper limb in a more functional position which can assist the patient with activities of daily living.
Conflict of interest/funding None.
References 1. Terzis JK, Papakonstantinou CK. The surgical treatment of brachial plexus injuries in adults. Plast Reconstr Surg 2000;106:1097e122. 2. Tung HT, Mackinnon SE. Brachial plexus injuries. Clin Plast Surg 2003;30:269e87. 3. Terzis JK, Kostopoulos V. The surgical treatment of brachial plexus injuries in adults. Plas Reconstr Surg 2007;119:73e92. 4. Doi K, Sakai K, Fuchigami Y, Kawai S. Reconstruction of irreparable brachial plexus injuries with reinnervated free-muscle transfer. J Neurosurg 1996;85:174e7. 5. Berger A, Becker HJ. Brachial plexus injuries: brachial plexus surgery: our concept of the last twelve years. Microsurgery 1994;15:760e7. 6. Perry J. Biomechanics and functional anatomy of the shoulder. In: Chapman WM, editor. Champan’s Orthopaedic surgery. 3th Ed. Philadelphia: Lippincott Williams and Wilkins; 2001. pp. 2063e2077. 7. Soames WR. Skeletal system. Shoulder (Glenohumeral)Joint. In: Williams LP, Bannister HL, et al., editors. Gray’s anatomy: the anatomical basis of medicine & surgery. 38th ed. Edinburg: Churchill Livingstone; 1995. p. 627e32. 8. Chuang DC, Gilbert WL, Fuad H, Wei FC. Restoration of shoulder abduction by nerve transfer in avulsed brachial plexus injury: evaluation of 99 patients with various nerve transfers. Plast Reconstr Surg 1995;96:122e8. 9. Terzis JK, Kostas I, Soucacos PN. Restoration of shoulder function with nerve transfers in traumatic brachial plexus palsy patients. Microsurgery 2006;26:316e24. 10. Terzis JK, Kostas I. Suprascapular nerve reconstruction in 118 cases of adult post traumatic brachial plexus. Plast Reconstr Surg 2006;117:613e27. 11. Terzis JK, Barmpitsioti A. Axillary nerve reconstruction in 176 posttraumatic plexopathy patients. Plast Reconstr Surg 2010; 125:233e47. 12. Aydin Y. Palliative surgery: tendons transfers to the shoulder in adults. In: Alain Gilbert, editor. Brachial Plexus injuries. London: Martin Dunitz; 2001. p. 111e22. 13. Leffert DR. Brachial plexus. In Green’s Operative hand surgery. 4th ed. Churchill Livingstone; 1999. 1557e1587. 14. Elhassan B, Bishop A, Shin A, Spinner R. Shoulder tendon transfer option for adult patients with brachial plexus injury. J Hand Surg 2010;35A:1211e9. 15. Terzis JK, Vekris MD, Soucacos PN. Outcomes of brachial plexus reconstruction in 204 patients with devastating paralysis. Plast Reconstr Surg 1999;104:1221e40. 16. Terzis JK, Kostopoulos VK. Free muscle transfer in posttraumatic plexopathies. Part 1: the shoulder. Ann Plast Surg 2010;65:312e7. 17. Rajiv M. Epidemiology of brachial plexus injuries in a multitrauma population. (Clinical studies). Neurosurgery 1997;40:1182e9. 18. Singh KA, Karki D. Modified trapezius transfer technique for restoration shoulder abduction in brachial plexus injury. Indian J Plast Surg 2007;40:39e45. 19. Mayer L. Transpantation of the trapezius for paralysis of the abductors of the arm. J Bone Jt Surg 1927;9:412e20. 20. Karev A. Trapezius transfer for paralysis of the deltoid. J Hand Surg 1986;11B:81e3.
Secondary shoulder reconstruction in patients with brachial plexus injuries 21. Milessi H. Brachial plexus injuries. In: Chapman WM, editor. Champan’s Orthopaedic surgery. 3th Ed. Philadelphia: Lippincott Williams and Wilkins; 2001. pp. 1703e1720. 22. Ruhmann O, Gosse F, Wirth CJ, Schmolke S. Reconstructive operations for the paralyzed shoulder in brachial plexus palsy: concept of treatment. Injury 1999;30:609e18. 23. Aziz W, Singer MR, Wolff WT. Transfer of the trapezius for the flail shoulder after brachial plexus injury. J Bone Jt Surg 1990;72B: 701e4. 24. Kotwal PP, Mittal R, Malhotra R. Trapezius transfer for deltoid paralysis. J Bone Jt Surg 1998;80B:114e6. 25. Monreal R, Paredes L, Diaz H, Pastor L. Trapezius transfer to treat flail shoulder after brachial plexus palsy. J Brach Plex Periph Nerv Inj 2007;2:2. 26. L’ Episcopo JB. Tendon transplantation in obstetrical paralysis. Am J Surg; 1934:122e5. 27. Freund KR, Terzis JK, Jordan L, Taylor G. Modified latissimus dorsi and teres major transfer for external rotation deficit of the shoulder. Orthop 1986;9:505e6. 28. Covey CD, Riordan CD, Milstead EM, Albritht AJ. Modification of the L’ Episcopo procedure for brachial plexus birth palsies. J Bone Jt Surg 1992;74B:897e901. 29. Pagnotta A, Haerle M, Gilbert A. Long term results on abduction and external rotation of the shoulder after latissimus dorsi transfer for sequelae of obstetric palsy. Clin Orthop Rel Res 2004;426:199e205. 30. Terzis JK, Kostopoulos E. Our experience with secondary reconstruction of external rotation in OBPP. Plast Reconstr Surg 2010;126(3):951e63.
853
31. Beauchamp M, Beaton DE, Barnhill TA, Mackay M, Richards RR. Functional outcomes after the L’Episcopo procedure. J Shoulder Elbow Surg 1998;7:90e6. 32. Ruhmann O, Gosse F, Schmolke S, Flamme C, Wirth CJ. Osteotomy of the humerus to improve external rotation in nine patients with brachial plexus palsy. Scand J Plast Reconstr Surg Hand Surg 2002;36:349e55. 33. Waters MP, Bae SD. The effect of derotational osteotomy on global shoulder function in brachial plexus birth palsy. J Bone J Surg 2006;88A:1035e42. 34. Terzis JK, Sweet RC, Dykes RW, Williams HB. Recovery of function in free muscle transplants using microneurovascular anastomosis. J Hand Surg 1978;3:37e59. 35. Bishop TA. Functioning free muscle transfer for brachial plexus injury. Hand Clin 2005;21:91e102. 36. Barrie AK, Steinmann PS, Shin YA, Spinner JR, Bishop TA. Gracilis free muscle transfer for restoration of function after complete brachial plexus. Neurosurg Foc 2004;16:1e8. 37. Chuang DC. Fuunctional free muscle transplantation for brachial plexus injury. Clin Orthop Relat Res 1995;314:104e11. 38. Itoh Y, Sasaki T, Ishiguro T, Uchinishi K, Yabe Y, Fukuda H. Transfer of latissimus dorsi to replace a paralyzed anterior deltoid. J Bone Jt Surg 1987;69B:647e51. 39. Hussl H, Huemer G. Transfer of pedicled musculocutaneous latissimus dorsi flap for restoration of shoulder contour after neurogenic atrophy. Ann Plast Surg 2007;58:694e7. 40. Richards RR, Waddell PJ, Hudson RA. Shoulder arthrodesis for the treatment of brachial plexus palsy. Clin Orthop Relat Res 1985;198:250e8.
Secondary shoulder reconstruction in patients with brachial plexus injuries* Julia K. Terzis a,*, Antonia Barmpitsioti b a
Department of Surgery, Division of Plastic and Reconstructive Surgery, Eastern Virginia Medical School (EVMS), 700 Olney Road, LH 2055, Norfolk, VA 23507, USA b Microsurgery Program, Department of Surgery, Eastern Virginia Medical School (EVMS), Norfolk, VA, USA Received 21 May 2010; accepted 28 December 2010
KEYWORDS Brachial plexus; Secondary shoulder reconstruction; Shoulder abduction; Free muscles transfers; Trapezius advancement; External rotation; Latissimus dorsi-teres major rerouting
Summary Restoration of shoulder stability in post-traumatic plexopathy patients is very important because more distal functions depend on a stable and functioning shoulder. The purpose of this study is to present our experience with secondary surgeries in patients with devastating paralysis. Functional outcomes were analyzed in relation to age, severity score and type of reconstruction. The medical records of 55 post-traumatic plexopathy patients who underwent secondary shoulder reconstruction, by a single surgeon, between 1978 and 2006, were reviewed. 55 patients had 73 procedures, 44 for shoulder abduction and 29 for external rotation. 38 patients underwent secondary surgery to augment shoulder abduction. Trapezius advancement was performed in 14 patients, double free muscle transfer in18, free latissimus dorsi in 4 and triceps muscle transfer in 2 patients. 26 patients had secondary procedures for enhancement of shoulder external rotation. Dynamic rerouting of latissimus dorsi and teres major was carried out in 18 patients and rotational humerus osteotomy in 11 patients. All patients had improvement of shoulder stability and function. Shoulder abduction reached 40.80 15.93 and external rotation at 24.28 17.90 . Trapezius advancement yielded 41.81 9.02 of abduction. Latissimus dorsi yielded stronger shoulder abduction than adductor longus. Rerouting of latissimus dorsi and teres major attained 22.33 20.31 of dynamic external rotation while humerus osteotomy produced 26.87 10.32 of external rotation. Secondary procedures such as pedicle and free muscles transfers, tendon transfers, and rotational humerus osteotomy augment shoulder stability and function in patients with irreparable paralysis. ª 2011 British Association of Plastic, Reconstructive and Aesthetic Surgeons. Published by Elsevier Ltd. All rights reserved.
* Informed consent was obtained from each patient. This study was reviewed and approved by the Eastern Virginia Medical School Institutional Review Board. * Corresponding author. E-mail address: [email protected] (J.K. Terzis).
1748-6815/$ - see front matter ª 2011 British Association of Plastic, Reconstructive and Aesthetic Surgeons. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.bjps.2010.12.015
844
J.K. Terzis, A. Barmpitsioti
Introduction
Table 2 Demographic data of 55 post-traumatic plexopathy patients.
Upper extremity palsy due to brachial plexus injuries have been described from antiquity. Surgical attempts to restore function in the injured upper extremity began early in the 20th century.1,2 Over the last 40 years a greater understanding of anatomy and pathophysiology of nerve regeneration, along with the introduction of microsurgery, allowed the development of strategies of reconstruction for brachial plexus injuries with feasible and predictable results.1e5 The shoulder is a complex of joints and muscles that connects the arm to the trunk. Its range of motion is performed by the coordinated movement of the glenohumeral, scapulothoracic, acromioclavicular and sternoclavicular joints which is called the scapulohumeral rhythm. For shoulder abduction-elevation approximately a 2:1 ratio of glenohumeral to scapulothoracic motion is required; 120 of abduction occurs at the glenohumeral joint and 60 at the scapulothoracic joint; the first 30 of abduction occurs mainly at the glenohumeral joint. The deltoid and supraspinatus muscles are the real abductors, while the infraspinatus, posterior deltoid and teres minor function as external rotators.6,7 Shoulder stabilization is very important as more distal motions such as elbow and hand require a stable shoulder for useful function. Lesions of the axillary and suprascapular nerves incapacitate shoulder abduction and external rotation. Primary nerve repair remains the “gold standard” in upper limb reconstruction.8e11 If surgery is early and successful, adequate reinnervation of deltoid, teres minor, supraspinatus and infraspinatus as well as glenohumeral joint stability can be achieved.10,11 Yet, when nerve repair is unsuccessful, or when the interval between injury and surgery is too long, secondary surgeries such as muscle and tendon transfers are needed to improve shoulder function and reduce shoulder subluxation.12e14 In the current study the senior authors’ experience with secondary shoulder reconstruction is presented. Functional outcomes were analyzed in relation to age, severity score and type of reconstruction.
Data
No of patients
Sex
Female: 8 Male: 47 Left: 32 Right: 22 Clavicle: 13 Scapula: 5 Ribs: 5 Axillary: 5 Subclavian: 5 Brachial: 1 25.49 8.66 8.18 5.83 (range 0e22) Normal plexus: 25 Global avulsion: 0 24.18 39.58 months 4.51 2.98
Patients and methods Between 1978 and 2006, a total of 55 patients with posttraumatic brachial plexus palsy underwent secondary shoulder reconstruction in our Center. The cause of the brachial plexus lesions in 49 patients was motor vehicle accidents (Table 1). The mean age was 25.49 8.66 years. Twenty two (22) patients had associated fractures (reconstruction took place elsewhere) and 11 had vascular injury. The demographic data is shown in Table 2. Table 1 Type of accident for 55 Post-traumatic Brachial Plexus Patients. Type of accident
No. of patients (%)
Motorcycle accident Motor vehicle accident Pedestrian Work related injury
31 (56.3%) 18 (32.7%) 3 (5.45%) 3 (5.45%)
Side Fractures
Vascular injury
Age (years) Severity score
Denervation time Follow-up (years)
Electrodiagnostic evaluation was performed in all patients while relevant angiography was carried out in patients scheduled for free muscle transfers. Meticulous clinical examination was performed in the entire upper extremity using a modified British Medical Research Council Grading System, expanded further with intermediate grades of þ and (e, g., M0 to M2 indicated poor result; M2þ to M3 was a fair result; M3þ to M4 indicated good result; and M4 to M5 was an excellent result).15 The values were recorded on a plexus chart. The passive and active range of shoulder motion was measured; shoulder abduction was measured against gravity starting with the arm at the side; shoulder external rotation was evaluated starting with the arm in the neutral position; the gained degrees of external rotation were measured and recorded. Additionally, preoperative and postoperative behavioral video analysis was carried out by three independent evaluators who viewed standardized videos separately and graded the results. The senior author (J. K. T.) introduced in 1984 a quantitative intraoperative scoring system that provides diagnosis of the brachial plexus lesion at the level of each root (Avulsion Z 0, Avulsion/Rupture Z 1, Rupture Z 2, Traction/Rupture Z 3, Traction Z 4, Normal Z 5). The total Table 3 Type of lesion for each root in 55 Post-traumatic Brachial Plexus Patients. Type of lesion
C5
C6
C7
C8
T1
Total
Avulsion Rupture/Avulsion Rupture Rupture/Traction Traction Normal
5 2 36 1 5 1
21 2 21 2 4 0
36 0 5 1 6 2
30 3 1 1 3 12
23 1 2 1 7 16
115 8 65 6 25 31
36 patients (65.45%) had severity score less than 10. Each root that has not been injured has a score of 5. The normal plexus has 25 severity score. The lower the severity score the worse the injury. There were 5 patients with infraclavicular lesions (9.09%).
Secondary shoulder reconstruction in patients with brachial plexus injuries Table 4
845
Donor nerve used for free muscles reinnervation.
Donor/Recipient
ACC
Cervical plexus
LD ADDL(SH) GRAC(EL)
6 3
4 6
C5
DRS
ICN
cLP
3 3 1
4
cC7
Other
1 4 3
1 1
Acc: Spinal accessory nerve; C5: C5 root; DRS: Dorsal scapular nerve; INC: Intercostal nerves; cLP: Contralateral Lateral Pectoral nerve; cC7: Contralateral C7 root; Other: Medial cord; LD, Latissimus dorsi; ADDL, Adductor longus; GRAC, Gracilis; SH, Shoulder; EL, Elbow.
Table 5
Type of secondary reconstruction in 55 patients with post-traumatic brachial plexus injuries.
Type of reconstruction
DFM
LD
Trap
Tric
PMJ- MI
cTrap
LD-TM
OS
No of patients
18
4
14
2
5
1
18
11
DFM: Double free muscles; LD: free latissimus dorsi; Trap: trapezius advancement; Tric: triceps; LD-TM: Rerouting of latissimus dorsiteres major; TM: teres major; PMJ- MI: pectoralis major- minor; OS: osteotomy; cTrap: contralateral trapezius. A combination of procedures such as free muscle and trapezius or pectoralis advancement took place in 6 patients while latissimus dorsi rerouting and humerus osteotomy was performed in 3 patients.
severity score for a normal plexus is 2515. The lower the severity score the worse the injury. The mean severity score in this series was 8.18 5.83 which reflects the severity of lesions in this patient population. There were 36 patients with severity score less than 10. A total of 115 root avulsions were encountered (Table 3). Primary reconstruction had been performed in 41 patients with axillary and/or suprascapular nerve repair; the resulting function was deemed not satisfactory and further procedures were needed to center the humerus into the glenoid and improve shoulder range of motion. In the current study, 55 patients had 73 procedures, 44 for shoulder abduction and 29 for external rotation. A total of 38 patients underwent reconstruction for restoration of shoulder abduction; in 14 patients the trapezius muscle was advanced for improvement of shoulder abduction; four patients had free contralateral latissimus dorsi transfer and 18 patients had double free muscle transfers, gracilis and adductor longus, for restoring simultaneously shoulder abduction and elbow flexion; the donor nerves for free muscle reinnervation are shown in Table 4. Secondary procedures for augmentation of shoulder external rotation were carried out in 26 patients; dynamic latissimus dorsi and teres major rerouting was
Figure 1 Intraoperative view of the free double muscle transfer prior to insetting.
performed in 18 patients. Rotational humerus osteotomy was performed in 11 patients (Table 5). 9 patients had secondary shoulder reconstruction to augment both abduction and external rotation and 9 patients had more than one procedure for strengthening shoulder stability and function, such as free muscle and trapezius or pectoralis minor advancement (n Z 6), latissimus dorsi rerouting and humerus osteotomy (n Z 3).
Surgical technique Adductor longus and gracilis transfer (Double Free Muscle Transfer) The senior author in 1983 introduced the double free muscle technique for both shoulder abduction and elbow flexion reanimation16. The gracilis was utilized for elbow flexion and the adductor longus for shoulder abduction. This transfer is based on their common vascular pedicle. The muscles were harvested through a curvilinear incision in the medial aspect of the thigh. The skin flaps are developed and the fascia incised to expose both muscles. The pedicle is identified as it enters the undersurface of the gracilis muscle but in this transfer the supplying branches to the adductor longus are preserved. Exploration of this common vascular pedicle leads to the profunda femoris vessels where the common pedicle will be taken. The obturator nerve is identified as it enters the gracilis muscle and intraoperative stimulation secures its integrity. This is traced proximally towards the inguinal ligament and the nerve to the adductor is encountered anterolaterally underneath the adductor longus. Once the neurovascular bundle is exposed both muscles are skeletonized. The common vascular pedicle is short while a respectable length of the supplying nerves 5e7cm can be taken. The muscles prior to transfer are tagged every one centimeter to mark the insitu tension. A second surgical team prepares the pocket in the paralyzed upper extremity where the double muscle unit is to be transferred. The difficulty with this procedure is that upon transfer, the adductor longus is placed laterally and the gracilis medially (see Figure 1). This places the common vascular
846
J.K. Terzis, A. Barmpitsioti
Figure 2 21 year old male was involved in a motor cycle accident. He sustained multiple injuries that lead to exploratory laparotomy, splenectomy, and trachiostomy. He also sustained pneumothorax, fracture of the left scapula, celebral contusion and left brachial plexus injury. 18 months later, the patient presented to our Center with impairment of shoulder abduction (Figure 2a). Exploration of plexus was carried out and microneurolysis of the entire plexus performed. Additionally banked nerves were placed from contralateral lateral pectoral (cLP), C2 and C3 motors and spinal accessory nerve. In another stage a double free muscle was transferred for simultaneous augmentation of elbow extension (gracilis) and shoulder abduction (adductor longus). Neurotisation was done by the cervical motors, C2, and C3 nerves. The patient 4 years later demonstrated 90 of shoulder abduction (Figure 2b).
Figure 3 Intraoperative photo of the contralateral free latissimus transfer prior to insetting.
pedicle laterally about 10e12 cm inferior to the acromion over the middle deltoid. As there are no recipient vessels at that site, long vein grafts are needed for the revascularization of the double muscle unit. The appropriate recipient vessels need to be prepared for end- to- side anastomoses prior to muscle transfer. Recipient vessels include the common carotid or the subclavian artery, and recipient veins include the subclavian, jugular or basilic veins. Insetting of the double muscle free flap is as follows: the gracilis is anchored to the lateral clavicle and the adductor longus to the acromion and spine of the scapula. Distally the gracilis is inserted in the distal biceps tendon, and the adductor longus on the lateral humerus on the deltoid groove and secured in place with compression screws. The original tension of the transplanted muscle units is restored by insetting the muscles with the insitu tension which was marked prior to transfer. Donor motor nerves for reinnervation of the double muscles included: distal spinal accessory,
Figure 4 31 year old male sustained an injury while motorcycle racing. He fell off his motorcycle and struck a wall with tires. He experienced loss of consciousness, right lung contusion, right fifth metacarpal fracture, and right brachial plexus palsy. He was referred to our Center 3 months later with a paralyzed right upper extremity (Figure 4a). Brachial plexus exploration revealed C5 rupture, C6-C7 avulsion and C8-T1 traction. The first stage of reconstruction included: Direct neurotisation of distal spinal accessory to suprascapular nerve, and C4 motor nerve and C5 root to posterior cord with interposition nerve grafts. In the second stage T8, T9 and T10 intercostal nerves neurotized directly the musculocutaneous nerve, T6 and T7 intercostals the long thoracic and T3-T4 intercostals the thoracodorsal nerve; T5 was used as banked nerve. 14 months later the right latissimus dorsi was transferred to augment elbow flexion and the right trapezius was transferred to augment shoulder abduction; humerus rotational osteotomy was also done to increase external rotation, and Steindler flexoplasty to augment elbow flexion. Wrist fusion and tendon transfers were performed 2 years later. The patient after the trapezius transfer presented with 80 of shoulder abduction (Figure 4b).
Secondary shoulder reconstruction in patients with brachial plexus injuries
847
Table 6 Results after secondary shoulder reconstruction (means SD) in 45 evaluated patients with post-traumatic brachial plexus palsy. Total patients with secondary shoulder reconstruction
Shoulder abduction degrees (means SD)
Shoulder external rotation degrees (means SD)
Pre-operative Post-operative Patients after primary reconstruction Pre-operative Post-operative
14.67 12.71 40.80 15.93
8 10.05 24.28 17.90
15.22 12.86 40 17.66
10.71 10.71 26.66 20.14
*The results (preoperative versus postoperative) were statistical significant for all groups (ManneWhitney test, p < 0. 001).
Table 7
Evaluated Functional outcomes versus different motor donor nerves used for free muscle reinnervation.
Donors (number of patients)
Free muscle grading (median, minimumemaximum)
Degrees of shoulder abduction (means SD)
Accessory (n Z 5) Cervical plexus (n Z 4) Intercostal (n Z 2) Dorsal scapular (n Z 3) Contralateral lateral pectoral (n Z 3)
2.33(1.66e3.33) 2.66 (1.33e3.33) 2.33 2.00 (1.33e3.00) 2.33 (1.33e2.33)
9 16.25 5 16.66 6.66
Preop
postop
13.41 12.50 7.07 15.27 11.54
40 15.41 38.33 5.77 30 35 21.79 26.66 5.77
Preop: preoperative; postop: postoperative. Difference between the donors was not statistically significant (KruskaleWallis test, p > 0.05).
Figure 5 Muscle grading versus different motor donor nerves used for free muscle reinnervation (means SD). A: spinal accessory nerve; B: cervical plexus motor donors; C: intercostal nerves; D: dorsal scapular nerve; E: (cLP)contralateral lateral pectoral nerve. Differences between motor donors were not statistically significant (KruskaleWallis test, p > 0.05).
cervical plexus motors, and contralateral lateral pectoral (cLP), (Table 4), (Figures 1 and 2). Latissimus dorsi The latissimus dorsi is harvested through a curved 20 cm incision starting at the axilla and running obliquely toward the posterior iliac spine. The origin of the muscle is
attached proximally along the nuchal line and the spinous processes of the cervical and upper thoracic spine. The distal tendon is secured on the lateral humerus on the deltoid groove. Compression screws are used for solid insetting. Transferring the latissimus dorsi, may on occasion result in webbing in the neck. Correction of this problem was by creation of a pulley, using fascia lata, which is secured on the spinous processes posteriorly to the clavicle anteriorly. The vascular pedicle is long and reaches the axillary or brachial artery. End- to- side anastomoses are performed. The donor nerves included direct intercostal neurotization (3 cases) and one case with the posterior division (PD) of contralateral C7 (cC7), (Table 4), (Figure 3). Trapezius advancement The trapezius is harvested through a curved supraclavicular incision. The lateral clavicular, acromial and spinous insertions of the trapezius are severed and the muscle is mobilized proximally and cranially. The transposed muscle is anchored with two screws in the deltoid insertion on the humerus. Usually, the trapezius needs to be elongated using a strip of fascia lata (Figure 4).
Table 8 Results after different types of reconstruction for shoulder abduction in 45 evaluated patients with post-traumatic brachial plexus palsy. Shoulder function/ Type of reconstunction
Muscle grading (median, minimum-maximum)
Shoulder abduction degrees (means SD) preop
postop
Double free muscles Free Latissimus dorsi Trapezius Advancement
2.33 (1.33e3.33) 2.33 (2.33e3.33) 2.66 (1.33e3.33)
14.33 13.34 3.33 5.77 16.81 12.70
36 13.12 41.66 20.88 41.81 9.02
Preop: preoperative; postop: postoperative. Difference between the types of reconstruction was not statistically significant (KruskaleWallis test p > 0.05).
848
J.K. Terzis, A. Barmpitsioti Postoperative, after free muscle transfer, intensive monitoring for 3 days can prevent postoperative vascular problems. Thus early diagnosis and immediate return to surgery will salvage the free muscle. The upper limb is immobilized in a prefabricated splint for 8 weeks with the arm in 90 abduction and elbow flexion. The splint is gradually adjusted to 60 and then 30 abduction and removed at three months. At six weeks following surgery the patients are fitted with a slow-pulse stimulator which they use five to six times a day. This stimulation protocol is continued until reinnervation takes place.
Statistical analysis
Figure 6 Diagrammatic depiction of the latissimus dorsi and teres major rerouting procedure for dynamic external rotation restoration.
The statistical analysis was performed with the assistance of the Department of Biostatistics of Eastern Virginia Medical School and using the Instat version 3.00 (GraphPad Software, SanDiego, Calif.). The results are presented as means SD and the muscle grading as median (minimum-maximum). Comparison of results was carried out using the ManneWhitney U test and between more than two groups using the KruskalWallis test. P values <0.05 were considered to be significant.
Figure 7 30 year old male sustained a high velocity motorcycle accident, in a collision with a truck. He was wearing a helmet. He experienced loss of consciousness, closed head injury, fracture of the left femur, fracture of the left wrist and fifth metacarpal and a global left brachial plexus palsy. He had previous brachial plexus exploration and reconstruction in another center and had some return of shoulder abduction but no external rotation. He was referred to our center 5 years after the accident (Figure 7a). The intraoperative findings were: rupture of C5, C6, and T1 and avulsion of C7 and C8. Reconstruction in our Center included: T5-T6 to thoracodorsal nerve; T7-T8 to triceps nerve; 75% of the proximal long thoracic to triceps nerve via a short graft; The phrenic nerve (one third), and 75% of the dorsal root of C5 to deep saphenous graft as banked nerve for finger flexors; and the distal accessory to left sural for finger extensors; T5-T6-T7 (sensory) were transferred to the median nerve for restoration of protective sensation to the hand. Furthermore release of pectoralis major and conjoin tendon (right shoulder arthroplasty) was performed followed by rerouting of the right latissimus dorsi and teres major for restoration of shoulder external rotation along with left wrist fusion. One year later, T3, T4, T9, T10 intercostal nerves were used as banked nerves and the left free gracilis was transferred for finger flexion; eight months later, the right gracilis was transferred for finger extension. 3 years later the patient demonstrated excellent shoulder function (fig. 7b) and almost full shoulder external rotation (Figure 7c).
Secondary shoulder reconstruction in patients with brachial plexus injuries
849
Figure 8 24 year old male was involved in a motorcycle accident. He fell on a car exiting a small road because the car violated a stop sign and he hit the side of the car with his body. He experienced unconsciousness and he sustained: right mandibular, left clavicle, left scapula, right thumb fractures; partial dislocation of T7-T8 vertebrae with paraplegia, left subclavian artery injury and left brachial plexus palsy. 23 months following the accident he was referred to our Center with upper plexus palsy (Figure 8a). Plexus exploration revealed C5 and C6 roots traction. The reconstruction at that time included: microneurolysis of C5, C6 roots, upper truck, and suprascapular nerve; A small segment of C5 was used to reconstruct the axillary with the use of interposition nerve grafts; to augment shoulder external rotation rerouting of latissimus dorsi and teres major was carried out. 4 years later the patient had excellent shoulder external rotation (Figure 8b).
Results 41 patients had previously primary nerve reconstruction with inadequate results. Functional outcomes were analyzed in 45 patients who had at least 2 years of followup; the mean follow-up was 4.51 2.98 years. Postoperative evaluation took place at 6 and 12 month intervals. All patients achieved a stable shoulder and in all patients the range of motion was improved (Table 6). Patients with ages less than 20 years obtained superior shoulder abduction (41.45 17.47 ) than older patients (36.66 9.85 ), (ManneWhitney test, p < 0.8); the difference was not statistically significant. Patients with severity score higher than ten regained significant better shoulder abduction (46.66 22.77 ) than patients with severity score less than ten, who regained 38.40 10.95 of abduction (ManneWhitney, p < 0.04). Evaluation of muscle transfers to reinforce shoulder abduction demonstrated that free latissimus dorsi transfer yielded stronger shoulder abduction (median 2.33(2.33e3.33), and 41.66 20.2 of abduction), than adductor longus as double free muscle transfer, which yielded median: 2.33(1.33e3.33) and 36 13.12 of abduction; this difference was not statistically significant (ManneWhitney, p < 0.52). The results from different motor donors are presented in Table 7 and Figure 5. Trapezius muscle advancement achieved median muscle grading 2.66(1.33e3.33), and 41.81 9.02 of shoulder abduction; trapezius muscle, before its advancement, had median grading 4.66, and the shoulder had full passive range of motion (Table 8). To assess the results of external rotation, the difference between the preoperative presentation of the patient, during which the arm was hold in internal rotation and the degrees of external rotation achieved postoperative were recorded; patients with latissimus dorsi and teres major rerouting attained a mean of 22.33 20.31 of external rotation (Figures 6,7 and 8). Humerus rotational osteotomy
yielded a mean of 26.87 10.32 of external rotation (Figures 9,10 and 11). Dynamic shoulder abduction and external rotation was also graded by three independent reviewers who reviewed separately preoperative and postoperative standardized videos of each patient. A total of 99 estimations were carried out for shoulder abduction and 45 for external rotation. There were 51.51% of estimations with more than 30 of abduction, and 46.66% of estimations with more than 15 of external rotation (Figure 12).
Discussion Rajiv17 noticed that brachial plexus injuries affect more than 1% of multitrauma victims; motor cycle injuries comprise 4.2% of brachial plexus damages while 0.67 of motor vehicle victims suffered brachial plexus injuries. The high impact of motor cycle accident can be explained by the increased forces applied to the neck area.1 In our series 75% of patients were involved in high velocity motor vehicle accidents.
Figure 9 Functional results for shoulder external rotation (degrees, means SD) by different types of reconstruction preoperative and postoperative. Differences were statistically significant for both procedures (ManneWhitney test p < 0.003). LD-TM: Latissimus and teres major rerouting procedure.
850
J.K. Terzis, A. Barmpitsioti
Figure 10 This 26 year old male was involved in a motorcycle accident. He was un-helmeted while he struck a bus door with his right side. He sustained the following: loss of consciousness, laceration of the right neck, closed head injury, lung contusion, paralysis of right hemidiaphragm, right tibial fracture, four ribs fracture, and right brachial plexus palsy. 4 months later he underwent brachial plexus exploration overseas. He was referred to our Center 12 months after the accident. His right shoulder was internally rotated and the forearm was held in pronation (Figure 10a). The intraoperative findings were: C5, C6, C7, C8 roots avulsion, T1 root traction. The reconstruction included: Direct neurotisation of the distal accessory nerve to suprascapular; T8, T9 intercostal nerves to axillary nerve; T6, T7, T10 intercostal nerves to musculocutaneous nerve; cC7 root posterior division (PD) via sural nerve grafts to triceps. Secondary reconstruction took place one year later involving tendon transfers for hand reanimation and humerus rotational osteotomy to improve shoulder external rotation. A final stage of reconstruction, 18 months later, involved a trapezius muscle transfer to augment shoulder abduction and wrist fusion. The patient seen at 6 years after the accident demonstrated reversal of the pronation deformity of his right arm (Figure 10b), and good external rotation (Figure 10c).
In Upper Brachial plexus lesions, primary repair of the axillary and suprascapular nerves is the treatment of choice yielding superior results especially in younger patients and when the interval between injury and surgery is short.9e11 Secondary procedures are carried out in cases of delayed presentation and when functional outcomes after primary reconstruction are inadequate.12e14 In this series, 41 patients underwent augmentation of primary reconstruction and all patients had prolonged denervation time (24.18 39.58 months) and multiple root avulsions (8.18 5.83 severity score). Secondary reconstructive strategies depend on the type of the brachial plexus lesion, the availability of local muscles,
good passive shoulder mobility, and at least M4 muscle grading as the transferable muscles always lose one muscle grade upon transfer. Procedures using a variety of muscles have been described.1214 The trapezius muscle transfer has been used since the early 20th century to augment shoulder stability.1820 Mayer19 transferred the trapezius for paralyzed abductors in six patients with gratifying results in four patients. Milessi21 reported that control of shoulder function can be achieved by transferring the trapezius with its bony insertion at the acromion onto the humerus. In Ruhmann’s22 series 82.6% of patients who experienced trapezius transfer expressed their satisfaction from the achieved shoulder stability and
Secondary shoulder reconstruction in patients with brachial plexus injuries
851
Figure 11 This is a 50 year old male who was involved in a high velocity vehicular accident. He was driving the truck; his left arm hit a metal bar. He experienced lost of consciousness and respiratory arrest. He furthermore sustained open wound trauma on the left shoulder and the left chest; fracture of the left ribs, open fracture of the left humerus, and fracture of the left radius, and ulnar; dislocation of the sternoclavicular joint; brachial artery injury; laceration of the face; and left brachial plexus palsy. 8 and ½ months later he presented to our center with a paralyzed left arm internally rotated (Figure 11a). The intraoperative findings included: traction of the left brachial plexus and rupture of the axillary and radial nerves. Extensive microneurolysis was performed as well as reconstruction of axillary and radial nerves. 9 months later the ipsilateral latissimus was transferred as a pedicle flap for elbow flexion, wrist fusion was performed, and bone graft was placed in the humerus fracture area. 2 and ½ years later 30 rotational osteotomy of the humerus was carried out to improve external rotation along with tendon transfers to improve hand function. The patient in a late follow-up (ten years later) demonstrated the gained external rotation and the good position of his upper extremity (Figure 11b).
function. Although Singh18 reported that performing trapezius transfer, patients regained a mean of 116 of shoulder abduction, most authors that used this transfer reported that the improvement of shoulder abduction ranged from 39 to
Figure 12 Preoperative and postoperative dynamic video evaluation for shoulder abduction and external rotation (degrees, means SD); assessment was carried out by three independent investigators. Preoperative the mean shoulder abduction and external rotation was 9.07 18.08 and 11.70 25.30 respectively, and postoperative the shoulder abduction was 39.64 37.14 and external rotation was 26.70 29.72 . Differences were statistically significant (ManneWhitney test, p < 0.006).
60 2225. In our series trapezius transfer yielded a mean of 41.81 9.02 of shoulder abduction. L’Episcopo26 in 1930 described the use of teres major and latissimus dorsi to restore shoulder external rotation in obstetric brachial plexus paralysis (OBPP). Modifications of this procedure have also been reported27,28. Good passive external rotation is a requirement. This procedure is wellestablished in OBPP patients.29,30 Beaucamp31 performed L’Episcopo procedure in 11 adult plexopathy patients and achieved a mean of 28 of external rotation. In the experience of the senior author, the rerouting of latissimus tendon around the humerus yields much better results in children than in adults.30 In this series, the adult patients who underwent this surgery achieved 22.33 20.31 of shoulder external rotation. Where there is a paucity of local muscles for dynamic external rotation restoration, humerus rotational ostetomy is recommended for posture correction32,33. Ruhmann32 using osteotomy in 9 patients with brachial plexus palsy reported 42 of external rotation as well as better upper extremity placement. In the present series the patients who had humerus osteotomy regained a mean of 26.87 10.32 of external rotation, with improvement in upper limb position and appearance. In the 1970’s, a lot of the principles of free muscle transfer were elucidated, which allowed the transfer of a healthy
852 normal muscle to a paralyzed extremity to become a viable reconstructive option.34 The selection of donor muscle depends on the type of blood supply, the length, volume, shape of muscle, architecture of muscles fiber, and force of contraction.35 To restore shoulder abduction by free muscle transfer remains one of the most challenging procedures in reconstructive surgery; the majority of authors use free muscle, mainly to enhance elbow and hand function3537. According to Chuang,37 functional free muscle transplantation for restoration of shoulder function was ineffective because of its complexity; he reported 4 patients where he performed free gracilis transfer to replace the deltoid or supraspinatus muscles and achieved only 20 of shoulder abduction. Itoh38 described a pedicle latissimus transfer to replace the anterior deltoid in 10 patients and in six patients achieved 90 of anterior flexion. Hussl39 used pedicle latissimus dorsi to improve the shoulder’s shape and appearance. The senior author introduced in 1983 the double free muscle transfer-gracilis and adductor longus- for simultaneous shoulder and elbow reconstruction, based on their common vascular pedicle. It is a difficult procedure as long interposition vein grafts are needed for revascularization, and there is a large discrepancy (5e1) in the vessel diameter between vein graft and vascular pedicle. Nevertheless, with one operation two functions can be restored. In our center this procedure was used from 1983 to 1992. Subsequently because of greater demands as far as muscle power in the Caucasian patient, larger muscles were used, and gracilis was used mainly for hand reanimation. Free latissimus transfer achieved stronger glenohumeral joint abduction but occasionally neck webbing occurred. The use of fascia lata as pulley provided a solution.1,3,16 One advantage of the procedure is that one can still use trapezius advancement in patients who need more powerful abduction. In this series, patients with free latissimus transfer regained a mean of 41.66 20.2 of abduction. Shoulder arthrodesis was recommended in the past as a well-recognized procedure to restore shoulder stability in patients with devastating paralysis.2,5,13,14,40 The senior author (J. K. T.), does not advocate glenohumeral joint fusion, because of its high complication rate and pain sequelae; on the contrary she advocates primary reconstruction of the brachial plexus, which if done in a timely manner, will restore useful shoulder stability and function.1,3 In late cases, free muscle transfers provide better function, less complications and can be combined with other procedures (like trapezius advancement) to further strengthen shoulder abduction.
Conclusion Restoration of shoulder stability is very important in patients with brachial plexopathies prior to pursuing reanimation of the forearm and hand. Secondary procedures can provide shoulder stabilization and improved function when results after primary reconstruction are inadequate or in late cases with long denervation time. Trapezius advancement and/or free muscle transfers can augment shoulder abduction and improve shoulder stability. Rerouting of latissimus and teres major can restore some dynamic external rotation. If local muscles are not available, rotational osteotomy of the
J.K. Terzis, A. Barmpitsioti humerus can place the paretic upper limb in a more functional position which can assist the patient with activities of daily living.
Conflict of interest/funding None.
References 1. Terzis JK, Papakonstantinou CK. The surgical treatment of brachial plexus injuries in adults. Plast Reconstr Surg 2000;106:1097e122. 2. Tung HT, Mackinnon SE. Brachial plexus injuries. Clin Plast Surg 2003;30:269e87. 3. Terzis JK, Kostopoulos V. The surgical treatment of brachial plexus injuries in adults. Plas Reconstr Surg 2007;119:73e92. 4. Doi K, Sakai K, Fuchigami Y, Kawai S. Reconstruction of irreparable brachial plexus injuries with reinnervated free-muscle transfer. J Neurosurg 1996;85:174e7. 5. Berger A, Becker HJ. Brachial plexus injuries: brachial plexus surgery: our concept of the last twelve years. Microsurgery 1994;15:760e7. 6. Perry J. Biomechanics and functional anatomy of the shoulder. In: Chapman WM, editor. Champan’s Orthopaedic surgery. 3th Ed. Philadelphia: Lippincott Williams and Wilkins; 2001. pp. 2063e2077. 7. Soames WR. Skeletal system. Shoulder (Glenohumeral)Joint. In: Williams LP, Bannister HL, et al., editors. Gray’s anatomy: the anatomical basis of medicine & surgery. 38th ed. Edinburg: Churchill Livingstone; 1995. p. 627e32. 8. Chuang DC, Gilbert WL, Fuad H, Wei FC. Restoration of shoulder abduction by nerve transfer in avulsed brachial plexus injury: evaluation of 99 patients with various nerve transfers. Plast Reconstr Surg 1995;96:122e8. 9. Terzis JK, Kostas I, Soucacos PN. Restoration of shoulder function with nerve transfers in traumatic brachial plexus palsy patients. Microsurgery 2006;26:316e24. 10. Terzis JK, Kostas I. Suprascapular nerve reconstruction in 118 cases of adult post traumatic brachial plexus. Plast Reconstr Surg 2006;117:613e27. 11. Terzis JK, Barmpitsioti A. Axillary nerve reconstruction in 176 posttraumatic plexopathy patients. Plast Reconstr Surg 2010; 125:233e47. 12. Aydin Y. Palliative surgery: tendons transfers to the shoulder in adults. In: Alain Gilbert, editor. Brachial Plexus injuries. London: Martin Dunitz; 2001. p. 111e22. 13. Leffert DR. Brachial plexus. In Green’s Operative hand surgery. 4th ed. Churchill Livingstone; 1999. 1557e1587. 14. Elhassan B, Bishop A, Shin A, Spinner R. Shoulder tendon transfer option for adult patients with brachial plexus injury. J Hand Surg 2010;35A:1211e9. 15. Terzis JK, Vekris MD, Soucacos PN. Outcomes of brachial plexus reconstruction in 204 patients with devastating paralysis. Plast Reconstr Surg 1999;104:1221e40. 16. Terzis JK, Kostopoulos VK. Free muscle transfer in posttraumatic plexopathies. Part 1: the shoulder. Ann Plast Surg 2010;65:312e7. 17. Rajiv M. Epidemiology of brachial plexus injuries in a multitrauma population. (Clinical studies). Neurosurgery 1997;40:1182e9. 18. Singh KA, Karki D. Modified trapezius transfer technique for restoration shoulder abduction in brachial plexus injury. Indian J Plast Surg 2007;40:39e45. 19. Mayer L. Transpantation of the trapezius for paralysis of the abductors of the arm. J Bone Jt Surg 1927;9:412e20. 20. Karev A. Trapezius transfer for paralysis of the deltoid. J Hand Surg 1986;11B:81e3.
Secondary shoulder reconstruction in patients with brachial plexus injuries 21. Milessi H. Brachial plexus injuries. In: Chapman WM, editor. Champan’s Orthopaedic surgery. 3th Ed. Philadelphia: Lippincott Williams and Wilkins; 2001. pp. 1703e1720. 22. Ruhmann O, Gosse F, Wirth CJ, Schmolke S. Reconstructive operations for the paralyzed shoulder in brachial plexus palsy: concept of treatment. Injury 1999;30:609e18. 23. Aziz W, Singer MR, Wolff WT. Transfer of the trapezius for the flail shoulder after brachial plexus injury. J Bone Jt Surg 1990;72B: 701e4. 24. Kotwal PP, Mittal R, Malhotra R. Trapezius transfer for deltoid paralysis. J Bone Jt Surg 1998;80B:114e6. 25. Monreal R, Paredes L, Diaz H, Pastor L. Trapezius transfer to treat flail shoulder after brachial plexus palsy. J Brach Plex Periph Nerv Inj 2007;2:2. 26. L’ Episcopo JB. Tendon transplantation in obstetrical paralysis. Am J Surg; 1934:122e5. 27. Freund KR, Terzis JK, Jordan L, Taylor G. Modified latissimus dorsi and teres major transfer for external rotation deficit of the shoulder. Orthop 1986;9:505e6. 28. Covey CD, Riordan CD, Milstead EM, Albritht AJ. Modification of the L’ Episcopo procedure for brachial plexus birth palsies. J Bone Jt Surg 1992;74B:897e901. 29. Pagnotta A, Haerle M, Gilbert A. Long term results on abduction and external rotation of the shoulder after latissimus dorsi transfer for sequelae of obstetric palsy. Clin Orthop Rel Res 2004;426:199e205. 30. Terzis JK, Kostopoulos E. Our experience with secondary reconstruction of external rotation in OBPP. Plast Reconstr Surg 2010;126(3):951e63.
853
31. Beauchamp M, Beaton DE, Barnhill TA, Mackay M, Richards RR. Functional outcomes after the L’Episcopo procedure. J Shoulder Elbow Surg 1998;7:90e6. 32. Ruhmann O, Gosse F, Schmolke S, Flamme C, Wirth CJ. Osteotomy of the humerus to improve external rotation in nine patients with brachial plexus palsy. Scand J Plast Reconstr Surg Hand Surg 2002;36:349e55. 33. Waters MP, Bae SD. The effect of derotational osteotomy on global shoulder function in brachial plexus birth palsy. J Bone J Surg 2006;88A:1035e42. 34. Terzis JK, Sweet RC, Dykes RW, Williams HB. Recovery of function in free muscle transplants using microneurovascular anastomosis. J Hand Surg 1978;3:37e59. 35. Bishop TA. Functioning free muscle transfer for brachial plexus injury. Hand Clin 2005;21:91e102. 36. Barrie AK, Steinmann PS, Shin YA, Spinner JR, Bishop TA. Gracilis free muscle transfer for restoration of function after complete brachial plexus. Neurosurg Foc 2004;16:1e8. 37. Chuang DC. Fuunctional free muscle transplantation for brachial plexus injury. Clin Orthop Relat Res 1995;314:104e11. 38. Itoh Y, Sasaki T, Ishiguro T, Uchinishi K, Yabe Y, Fukuda H. Transfer of latissimus dorsi to replace a paralyzed anterior deltoid. J Bone Jt Surg 1987;69B:647e51. 39. Hussl H, Huemer G. Transfer of pedicled musculocutaneous latissimus dorsi flap for restoration of shoulder contour after neurogenic atrophy. Ann Plast Surg 2007;58:694e7. 40. Richards RR, Waddell PJ, Hudson RA. Shoulder arthrodesis for the treatment of brachial plexus palsy. Clin Orthop Relat Res 1985;198:250e8.