Journal Pre-proof Outcomes of Reconstructive Surgery in Traumatic Brachial Plexus Injury with Concomitant Vascular Injury Alice E. Huang, BS, Shelley S. Noland, MD, Robert J. Spinner, MD, Allen T. Bishop, MD, Alexander Y. Shin, MD PII:
S1878-8750(19)33016-5
DOI:
https://doi.org/10.1016/j.wneu.2019.11.166
Reference:
WNEU 13835
To appear in:
World Neurosurgery
Received Date: 10 September 2019 Revised Date:
27 November 2019
Accepted Date: 28 November 2019
Please cite this article as: Huang AE, Noland SS, Spinner RJ, Bishop AT, Shin AY, Outcomes of Reconstructive Surgery in Traumatic Brachial Plexus Injury with Concomitant Vascular Injury, World Neurosurgery (2020), doi: https://doi.org/10.1016/j.wneu.2019.11.166. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Elsevier Inc. All rights reserved.
Outcomes of Reconstructive Surgery in Traumatic Brachial Plexus Injury with Concomitant Vascular Injury
Running title: TBPI Vascular Alice E. Huang, BS1 Shelley S. Noland, MD3 Robert J. Spinner, MD1,2 Allen T. Bishop, MD1,2 Alexander Y. Shin, MD1,2
ORIGINATING INSTITUTION: 1
Department of Orthopedic Surgery
2
Department of Neurologic Surgery, Mayo Clinic, Rochester, MN
3
Department of Plastic Surgery, Mayo Clinic, Scottsdale, AZ. Study performed at Mayo Clinic,
Rochester.
CORRESPONDING AUTHOR: Alexander Y. Shin, MD Department of Orthopedic Surgery Mayo Clinic 200 1st St SW Rochester, MN 55905 Telephone: 507-284-3689 Fax: 507-266-2533 Email:
[email protected] FINANCIAL MATERIAL & SUPPORT: Departmental funding was utilized without commercial sponsorship or support. RELEVANT CONFLICT(S) OF INTEREST TO DECLARE: None. INSTITUTIONAL REVIEW BOARD APPROVAL: IRB 17-011145 KEY WORDS: adult traumatic brachial plexus; surgical outcomes; vascular injury
TBPI Vascular 1 ABSTRACT Objectives: To investigate functional outcome from reconstructive surgery in adult traumatic brachial plexus injury (AT-BPI) with associated vascular lesions. Methods: A retrospective review was performed of 325 patients with AT-BPI who underwent reconstructive surgery between 2001 and 2012. Patients with (vascular) and without (control) vascular injuries were identified by review of medical documentation. Patient presentation, characteristics of nerve and associated lesions, and surgical management were evaluated to identify prognostic variables. Postoperative muscle strength, range of motion, and patientreported disability scores were analyzed to determine long-term outcome. Results: Sixty-eight patients had a concomitant vascular injury. There were no significant differences in age or sex between the control and vascular groups. Vascular patients were more likely to have pan-plexus lesions (p<0.0001), with significantly more associated upper extremity injuries (p<0.0001). The control group underwent more nerve transfers whereas vascular patients underwent more nerve grafting (p=0.003). Complete outcomes data were obtained in 139 patients, which included 111 control (43% of all controls) and 28 vascular patients (41%). There was no significant difference in patient-reported disability scores between the two groups. However, 73% of controls had grade 3 or greater postoperative elbow flexion while only 43% of vascular patients achieved these strengths (p=0.003). Control patients demonstrated a greater increase in strength of shoulder abduction as well (p=0.004). Shoulder external rotation strength was grade 0 in the majority of patients, with no difference between the two groups. Conclusions: Concomitant vascular injury leads to worse functional outcome following reconstructive surgery of traumatic brachial plexus injury.
TBPI Vascular 2 INTRODUCTION Adult traumatic brachial plexus injuries (AT-BPI) are devastating life altering injuries that result in significant physical disability, psychological distress, and socioeconomic hardship. These injuries result from a variety of etiologies, including penetrating injuries, falls, and motor vehicle trauma.1,2 Due to the high energy mechanisms of injury and anatomic proximity, associated injuries are common; these include spinal cord injury, fractures (clavicle, scapula, humerus, vertebrae, ribs, etc.) and vascular injuries.3–5 Knowledge regarding the incidence of vascular injuries in AT-BPI is limited and not well reported.4–8 Narakas et al reported that in 108 supraclavicular AT-BPI, 13% had a ruptured subclavian artery;4 in patients with infraclavicular AT-BPI, 41% had a ruptured axillary artery.4 Terzis et al. identified 57 patients out of 204 (28%) with a vascular injury, most commonly to the axillary artery.5 In 153 patients with infraclavicular AT-BPI, Chuang et al found that 23% had associated vascular injuries, primarily affecting the axillary artery.9 The outcomes of concomitant nerve and vascular injuries are rarely reported, generally not specific to AT-BPI, and often contradictory. Many authors suggest that outcomes of nerve reconstruction are worse when there is an associated vascular injury,10–13 whereas others disagree.14 It has been our anecdotal experience that AT-BPI patients with vascular injuries have poorer outcomes, more surgical complications/failures, and worse pain. Additionally, we suspect that the incidence of scapulothoracic dissociation is under-recognized in AT-BPI patients with vascular injuries. The purpose of this study is to evaluate the functional and patient-reported outcomes of AT-BPI reconstruction in patients with associated vascular injury as well as
TBPI Vascular 3 addressing the significance and impact of location and type of vascular injury and incidence of scapulothoracic dissociation.
METHODS After institutional review board approval, all patients with AT-BPI who underwent primary nerve reconstructive surgery by the senior authors (AYS, ATB RJS) between January 1, 2001 and December 31, 2012 were identified. Exclusion criteria included <16 years of age, previous brachial plexus reconstruction elsewhere, reconstruction of failed primary surgery, delayed reconstruction (presentation >1 year), and non-traumatic AT-BPI. Patients who were referred after greater than 1 year post injury were excluded as surgical options for primary nerve surgery have poorer outcomes that if performed prior to six months from.15,16 Diagnosis of AT-BPI was established by clinical evaluation, electrodiagnostic studies, cervical myelography, and surgical exploration (with intraoperative nerve action potentials (NAP), somatosensory evoked potentials (SSEP) and motor evoked potential (MEP) testing). Patients were classified as with or without associated vascular injuries based on review of operative reports, vascular imaging studies, clinical evaluation, and/or surgical exploration. Demographic data were recorded. AT-BPI was classified into 3 groups: upper trunk only (C5C6), upper trunk + C7, and pan-plexus. Associated ipsilateral injuries were recorded and organized as thoracic cavity injury (rib fractures, pneumothorax, pulmonary contusion), shoulder girdle injury (clavicle, scapula), upper extremity injury (non-shoulder girdle), lower extremity injury, and spinal fracture(s). Outcomes measures included muscle strength as measured by the modified British Medical Research Council (BMRC) scale, active range of motion (ROM), Disability of Arm-Shoulder-
TBPI Vascular 4 Hand Questionnaire (DASH) scores, and pain was measured using a Visual Analogue Scale (VAS) scale. Each senior author (AYS, ATB RJS) independently graded muscle strength, and a consensus grade was obtained if there was discrepancy. In order to obtain a BMRC grade 3, the patient had to have active motion against gravity equal to passive motion (Table 1). Additionally, a greater grade could not be obtained unless the criteria were met for the lower grade.17 The DASH score was normalized to a 1-100 grading scale with a higher score indicating greater disability.18 All brachial plexus reconstructive surgeries were performed by the senior authors (AYS, ATB RJS). All patients underwent exploration of the supraclavicular brachial plexus. Computerized tomographic myelogram, EMG, clinical exam and intraoperative MEP and SSEP were used to determine the level of injury, which was classified as described above. Types of nerve reconstruction included direct nerve repair, nerve grafting, nerve transfers, and free functioning muscle transfers (FFMT). All root injuries were confirmed using exploration and intraoperative nerve monitoring to confirm function prior to grafting. When vascular reconstruction was necessary at the time of reconstruction, a consistent vascular surgery team assisted in the reconstruction. The type of vascular reconstruction was determined by the vascular surgery team, with primary repair in uncomplicated cases and graft interposition or bypass for more extensive lesions. The presence of scapulothoracic dissociation, determined by measuring the distance between a midline thoracic spinous process and the medial border of the scapula of both injured and uninjured upper extremities, was recorded and classified according to Zelle et al (Table 2).19 No strict cutoff for a positive scapular index exists; however, any greater than 1.29 is consistent with scapulothoracic dissociation until proven otherwise.19-22
TBPI Vascular 5 Descriptive statistics for each study group are summarized as means and medians for continuous variables and counts and percentages for nominal variables. Analysis comparing DASH scores, BMRC grades, and ROM between the two groups utilized Fischer’s exact test for nominal variables and two-sample T tests for continuous variables. Significance was set at an α≤0.05.
RESULTS During the study period 325 patients had primary nerve reconstruction for AT-BPI; 281 were male (86%) and 44 were female (14%) (Table 3). The average age was 31 (range 16 to 69). Sixty-eight of the 325 patients (21%) had a concomitant vascular injury. There were no statistically significant differences in distribution of age or sex between the patients with and without concomitant vascular injury (p=0.33 & 0.22, respectively). The average follow-up duration was 25.1 months for control and 25.0 months for vascular patients (p=0.95). The most common etiology of injury was motor vehicle accident (84.3%) (Table 4). When compared to other etiologies, a fall from height more commonly resulted in AT-BPI without vascular injury (p=0.05). There was no significant difference between groups for injuries resulting from other etiologies (p=0.19-0.36) (see Table 4). A near majority of brachial plexus injuries in both groups were pan-plexus (58% overall) (Table 5). Upper trunk lesions and upper trunk + C7 lesions were both more common in the control group (p<0.0001 and 0.0003, respectively), whereas pan-plexus lesions were more common in the vascular group (p<0.0001). Spinal accessory nerve injury was documented in one case. There was no documentation of injury to the phrenic nerve. Associated ipsilateral injuries occurred in the upper extremity (38%), shoulder girdle (34%), thoracic cavity (32%), spine (24%), and lower extremity (20%) (Table 6). Upper extremity
TBPI Vascular 6 injuries, in particular humeral, radial, and ulnar fractures, were significantly higher in the vascular group (p<0.0001). Patients without any ipsilateral injuries were significantly more likely to have brachial plexus lesions without vascular injury (p=0.02). Vascular imaging at our institution was completed in 81 (32%) control and 52 (76%) vascular patients. The remainder of vascular patients who did not undergo vascular imaging had completed radiological workup at an outside institution at the time of vascular repair, notably immediately following the trauma. Magnetic resonance angiogram was the most common imaging modality (29% of control, 63% of vascular patients). In the vascular group, the subclavian artery was most commonly injured (44%), followed by the axillary (35%) and brachial (21%) arteries. Other locations of vascular injury included the radial artery, vertebral artery, internal carotid artery, and aortic arch. Some patients had multiple foci of vascular injury (n=7, 10% of vascular patients). Scapulothoracic dissociation (SD) occurred in 15 (4.6%) cases, including 10 (3.9%) control and 5 (7.4%) vascular patients (Table 7). There was no significant difference in incidence of SD between control and vascular groups (p=0.32). However, among those with SD, patients with concomitant vascular injuries were more likely to have Zelle 3 injuries while those without were more likely to be classified as Zelle 2B (p=0.01). Nerve reconstruction was completed in all 325 patients (Table 8). In control subjects, the most common procedure was nerve transfers (70%), while the majority of vascular patients underwent nerve grafting (79%) (p=0.003). Ninety-one (28%) patients received both nerve grafts and transfers. Use of an interposition graft was documented in 3 (1.3%) cases. Of the total of 219 nerve transfers performed in both control and vascular subjects, the types included triceps to axillary nerve (n=29; 13%), spinal accessory to suprascapular (n=77; 35%), single Oberlin procedure (n=47; 21%), double Oberlin procedure
TBPI Vascular 7 (n=51; 23%), intercostal to musculocutaneous (n=54; 25%), and other miscellaneous types (n=60; 27%). Sixty-four of the 68 vascular patients (94%) underwent repair for their vascular injuries (Table 9). All vascular reconstructions were performed on the day of injury at the institution of presentation; in all but 2 cases, these procedures occurred at an outside institution. Vessel grafts were performed in 63% of patients, vessel bypass in 23%, and primary arterial repair in 15%. The four patients who did not undergo vascular repair received pharmacological anticoagulation therapy (n=2), upper extremity amputation (n=1), or demonstrated arterial kinking that did not require repair (n=1). Of the 325 patients, complete BMRC, ROM, DASH, and VAS data were obtained in 139 patients. This subset of patients included 111 control patients (43% of all controls) and 28 vascular injury patients (41%). Of the 15 patients with SD, only 7 had full outcomes data; due to this small sample size, outcomes analysis comparing SD cases to non-SD cases was not performed. Preoperative, postoperative, and change in DASH and VAS scores were equivalent between control and vascular groups (Table 10). With regards to elbow flexion, the majority of each group (77% control, 89% vascular) initially presented with BMRC grade 0 elbow flexion (Table 11). There was no difference between the pre-operative distribution of BMRC grades for elbow flexion between control and vascular patients (p=0.31). However, following reconstructive surgery, 73% of control patients had grade 3 or greater elbow flexion while only 43% of vascular patients achieved these strengths (p=0.003). Furthermore, there was a significantly higher mean change in BMRC grades in control patients, with 2.5-point increase compared to a 1.8-point increase in those with vascular injuries (p=0.04).
TBPI Vascular 8 In terms of shoulder abduction, 71% of control and 64% of vascular patients presented with grade 0 strength (Table 12). Following surgery, 41% of control and 33% of vascular subjects demonstrated grade 3 or greater muscle strength. There were no significant differences in preoperative (p=0.89) or post-operative (p=0.68) BMRC grades for shoulder abduction between the two study groups. However, those without vascular injury demonstrated a significantly greater increase in strength of shoulder abduction (mean 1.4-point increase in BMRC grade) than those with vascular injuries (mean 0.9-point increase) (p=0.004). Shoulder external rotation presented initially as BMRC grade 0 in 77% of control and 79% of vascular patients (Table 13). There was no difference in distribution of preoperative, postoperative, or change in BMRC grades between the two study groups. Comprehensive ROM measurements are shown in Table 14. Post-operative ROM of elbow flexion was significantly greater in control patients (77° vs. 51° increase) (p=0.003). In terms of ROM of shoulder abduction and external rotation, there were no differences in pre-operative, post-operative, or change in ROM between the study groups.
DISCUSSION Brachial plexus lesions can often lead to significant physical disability and psychosocial distress. When concomitant vascular trauma is present, these injuries may lead to arm amputation or even death.23-26 According to major series reported in the literature, motor vehicle accidents are the most common cause of brachial plexus injuries,27,28 a trend reflected in the present study. Other causes include gunshot wounds, lacerations, and falling from a height; the prevalence of these etiologies are often influenced by socioeconomic factors such as wartime and political instability. 29-31 While the exact incidence of brachial plexus injuries is difficult to ascertain, the
TBPI Vascular 9 number of AT-BPI continues to rise every year due to advances in resuscitation measures resulting in increasing survivorship from motor vehicle accidents.4 The co-occurrence of brachial plexus and vascular injuries is common, with reported rates ranging from 10-35%.5,7,12,13 Blunt extremity trauma is often associated with bone fractures and joint dislocations, which can impact surrounding neurovasculature. As observed in the present study, the rates of vascular injury were significantly greater in patients with high energy injuries with associated upper extremity fractures. Vascular injury was also associated with a greater extent of neural injury, as reflected in the greater number of pan-plexus injuries in the vascular group. The spectrum of vascular injury can range from localized trauma to the subclavian vessels that do not require surgical intervention to the most severe injury of SD. Subclavian and axillary vessel lesions are the most prevalent vascular injuries associated with brachial plexus injuries, and more broadly, with upper extremity trauma.3,7,8,25,32 In our vascular cohort, subclavian vessel injury accounted for nearly half of the lesions. The presence of SD, an infrequent injury involving complete loss of scapulothoracic articulation with lateral scapula displacement and intact overlying skin, was also documented in our study. Oreck et al first described this condition in his 1983 case series.20 Since then, fewer than 100 well-documented cases have been published in the literature.19 SD has been shown to cause significant short- and long-term disability in patients with brachial plexus injuries.20,33-36 To determine the presence of SD, Zelle et al recommended measuring the distance between a midline thoracic spinous process and the medial border of the scapula of both the injured and uninjured upper extremities at the same level.19 Kelbel et al further developed this radiographic assessment by calculating a ratio of the distances on the injured and uninjured sides and comparing the results from patients with and without scapulothoracic dissociation.21 In the present cohort, there was no difference in SD
TBPI Vascular 10 incidence between the study groups. By nature of the classification system, the vascular group exhibited a greater number of Zelle 3 injuries while the control group had significantly more Zelle 2B (i.e. nonvascular) lesions. Unfortunately, due to the small number of SD cases with full outcomes data (n=7), statistical analysis of outcomes in this subset was unable to be performed. It would be reasonable to hypothesize that given the range in severity of possible vascular injuries, combining the entire spectrum of vascular injuries as a single pattern may result in a false reporting of the outcomes of brachial plexus reconstruction. Regarding the reconstructive strategy employed for nerve repair, it should be noted that in the present study, termination of the use of nerve grafts versus nerve transfers was made after intraoperative brachial plexus exploration and intraoperative nerve monitoring. If viable cervical roots were identified (i.e. no avulsion), grafts were incorporated into the overall reconstructive strategy. Frequently, the authors utilize both nerve grafts and nerve transfers in conjunction with functional muscle transfers to provide the best possible outcome. In our cohort, control patients more frequently underwent nerve transfers while vascular patients received more nerve grafts. While both are established reconstructive procedures, each has associated advantages, which may guide surgeons in choosing one over the other. Nerve grafting is typically performed when injury results in postganglionic nerve ruptures or neuromas that do not conduct a nerve action potential, but where the nerve has maintained viable motor axons that can be grafted to a target.1,2 Furthermore, interpositional grafts are necessary with longer lesions.37 However, nerve transfers typically demonstrate faster recovery and more specific regeneration than grafts.1,38 In a meta-analysis by Merrell et al including 1088 nerve transfers with and without interposition nerve grafts from 27 different studies, nerve transfers were shown to be effective for restoring elbow flexion to a BMRC grade 3 or greater in 72% of cases. In
TBPI Vascular 11 contrast, nerve grafting achieved these elbow flexion strengths in 47% of cases.39 The decision to perform a given procedure is influenced by several factors, and possibly guided by the mechanism and aftermath of the injury. Given the significantly higher number of associated upper extremity injuries (i.e. fractures) in the vascular group and associated soft tissue scarring, options for nerve transfers were limited and nerve grafting was often chosen to bypass the long segment of nerve injury. Because nerve grafting may be more commonly employed for extensive nerve injury, i.e. pan-plexus lesions, which in turn is more frequently seen with vascular injury, the increased use of nerve grafts may account for the worse functional outcome in our vascular cohort. The authors postulated that differences in functional outcome following reconstructive surgery for patients with concomitant vascular injury were due to insufficient vascularization. Previous studies have not concurred regarding the impact of associated vascular injury on long-term functional recovery from brachial plexus trauma. In a study of 407 ulnar nerve lesions caused by gunshot wounds, Secer et al reported no difference in functional outcome between patients with and without concurrent acute vascular injuries.40 Several studies report on the coexistence of ATBPI and various vascular injuries without comment on the outcomes in these two groups.7,8,12,41 The effect of concurrent vascular injury on the outcome of nerve injuries outside of the brachial plexus has received minimal attention. In a study of 151 upper limb injuries incurred from war, approximately one-third of the nerve injuries had concurrent arterial injuries. Functional recovery was obtained in only 44.8% of cases with combined neurovascular injury, an outcome at least partially attributable to nerve ischemia at the injury site.10,37,42 In an extensive military series from the Vietnam Vascular Registry, Rich et al found concurrent neurovascular injuries in 44% of patients. Despite successful vascular repair, the majority of cases with associated
TBPI Vascular 12 peripheral nerve injury suffered permanent functional deficit.43 In another study investigating acute trauma to peripheral arteries, patients with arm or leg arterial injury associated with nerve lesions were more likely to fail in regaining any motor or sensory function.44 The conclusion that nerve injury is the single most important factor in determining the degree of functional loss is prevalent in the vascular literature.44-47 In the present study, there was no significant difference in patient-reported functionality between the study groups. However, there was a significant objective improvement in capacity for elbow flexion in control patients when compared to those with vascular lesions, both in terms of higher rates of recovered antigravity function (i.e. BMRC grade 3 or higher) and increased range of motion. A significant functional difference between the groups was also detected with regard to shoulder abduction, though the improvement in ROM was less than with elbow flexion and without demonstrable difference between the groups. Prior studies have shown that though the strength of shoulder abduction improves following neurotization, even good results led to no greater than a 45 degree improvement in ROM.39 The movement that demonstrated poor recovery universally was external rotation of the shoulder, with nearly 50% of patients remaining at grade 0 function postoperatively in both study groups. Most surgeons consider restoration of elbow flexion as the highest priority when treating a flail extremity, followed by shoulder abduction and lastly distal sensation and motor capability.1 Unfortunately, persistent loss of external rotator function is commonly seen following AT-BPI regardless of whether reconstruction was performed.48,49 The present study is one of the larger studies evaluating the effect of concomitant vascular injury on functional recovery following reconstructive surgery for TBPI. We recognize the limitations of the study, which include a relatively small sample size, particularly of the vascular group.
TBPI Vascular 13 Furthermore, the majority of patients in both control and vascular groups were medically evaluated prior to referral to the authors’ institution. For patients deemed to have vascular injuries, these were often treated immediately and thus data such as time to revascularization, choice of vascular study, and management decisions were unavailable and unable to be controlled for within our dataset. The present study also operated on the assumption that each patient in the control group had no vascular injury. However, it must be acknowledged that incomplete injury such as stretch, intimal damage, or small dissections that did not prompt or did not manifest on vascular imaging was possible in these patients. Obtaining full outcomes data was also challenging and resulted in fewer (n=139) patients used for outcomes analysis due to incomplete patient-reported data (DASH and VAS surveys). Due to the nature of tertiary care centers receiving patients from varying geographical distances, many patients cannot return for consistent follow-up visits. Several failed attempts were made to contact patients postoperatively, resulting in incomplete survey data. Additionally, there was a lack of documentation of cold intolerance both objectively and subjectively. In order to fully capture the impact of concomitant vascular lesions on nerve construction outcomes, prospective longitudinal multi-institutional studies with agreed upon outcome measures including evaluation of cold intolerance is required. These limitations notwithstanding, the detrimental effect on functional outcome of a vascular injury associated with AT-BPI is elucidated in this study and can assist surgeons in counseling their patients.
TBPI Vascular 14
TBPI Vascular 15 Informed consent was obtained for experimentation with human subjects.
TBPI Vascular 16
REFERENCES 1.
Shin AY, Spinner RJ, Steinmann SP, Bishop AT. Adult traumatic brachial plexus injuries. J Am Acad Orthop Surg. 2005;13:382-396.
2.
Noland SS, Bishop AT, Spinner RJ, Shin AY. Adult Traumatic Brachial Plexus Injuries. J Am Acad Orthop Surg. Jan. 30 2019. [epub ahead of print] doi: 10.5435/JAAOS-D-1800433
3.
Rhee PC, Pirola E, Hebert-Blouin MN, et al. Concomitant traumatic spinal cord and brachial plexus injuries in adult patients. J Bone Jt Surg - Ser A. 2011;93:2271-2277.
4.
Narakas AO. Lesions found when operating traction injuries of the brachial plexus. Clin Neurol Neurosurg. 1993;95 Suppl:S56-S64.
5.
Terzis JK, Vekris MD, Soucacos PN. Outcomes of brachial plexus reconstruction in 204 patients with devastating paralysis. Plast Reconstr Surg. 1999;104:1221-1240.
6.
Goldie BS, Coates CJ. Brachial plexus injury: A survey of incidence and referral pattern. J Hand Surg Am. 1992;17:86-88.
7.
Sturm JT, Perry JF. Brachial plexus injuries from blunt trauma - A harbinger of vascular and thoracic injury. Ann Emerg Med. 1987;16:404-406.
8.
Johnson SF, Johnson SB, Strodel WE, Barker DE, Kearney PA. Brachial plexus injury: Association with subclavian and axillary vascular trauma. J Trauma - Inj Infect Crit Care. 1991;31:1546-1550.
9.
Lam WL, Fufa D, Chang NJ, Chuang DCC. Management of infraclavicular (Chuang Level IV) brachial plexus injuries: A single surgeon experience with 75 cases. J Hand Surg Eur Vol. 2015;40:573-582.
10.
Stanec S, Tonkovic I, Stance Z, Tonković D, Džepina I. Treatment of upper limb nerve
TBPI Vascular 17 war injuries associated with vascular trauma. Injury. 1997;28:463-468. 11.
Brown KR, Jean-Claude J, Seabrook GR, Towne JB, Cambria RA. Determinates of functional disability after complex upper extremity trauma. Ann Vasc Surg. 2001;15:4348.
12.
Graham JM, Mattox KL, Feliciano D V., DeBakey ME. Vascular injuries of the axilla. Ann Surg. 1982;195:232-238.
13.
Lin PH, Koffron AJ, Guske PJ, et al. Penetrating injuries of the subclavian artery. Am J Surg. 2003;185:580-584.
14.
Rasulic L, Cinara I, Samardzic M, et al. Nerve injuries of the upper extremity associated with vascular trauma—surgical treatment and outcome. Neurosurg Rev. 2017;40:241249.
15.
Nagano A, Tsuyama N, Ochiai N, Hara T, Takahashi M. Direct nerve crossing with the intercostal nerve to treat avulsion injuries of the brachial plexus. J Hand Surg Am. 1989;14:980-985.
16.
Songcharoen P, Mahaisavariya B, Chotigavanich C. Spinal accessory neurotization for restoration of elbow flexion in avulsion injuries of the brachial plexus. J Hand Surg Am. 1996;21:387-390. 17. Giuffre JL, Kakar S, Bishop AT, Spinner RJ, Shin AY. Current Concepts of the Treatment of Adult Brachial Plexus Injuries. J Hand Surg Am. 2010;35:678-688.
18.
Hudak PL, Amadio PC, Bombardier C, et al. Development of an upper extremity outcome measure: the DASH (disabilities of the arm, shoulder and hand) [corrected]. The Upper Extremity Collaborative Group (UECG). Am J Ind Med. 1996;29:602-608.
19.
Zelle BA, Pape HC, Gerich TG, Garapati R, Ceylan B, Krettek C. Functional Outcome
TBPI Vascular 18 Following Scapulothoracic Dissociation. J Bone Jt Surg - Ser A. 2004;86:2-8. 20.
Oreck SL, Burgess A, Levine AM. Traumatic lateral displacement of the scapula: A radiographic sign of neurovascular disruption. J Bone Jt Surg - Ser A. 1984;66:758-763.
21.
Kelbel JM, Jardon OM, Huurman WW. Scapulothoracic dissociation. A case report. Clin Orthop Relat Res. 1986;209:210-214.
22.
Lee L, Miller TT, Schultz E, Toledano B. Scapulothoracic dissociation. Am J Orthop. 1998;27:699-702.
23.
Millesi H. Surgical management of brachial plexus injuries. J Hand Surg Am. 1977;2:367-378.
24.
Galanakos SP, Zoubos AB, Ignatiadis I, Papakostas I, Gerostathopoulos NE, Soucacos PN. Repair of complete nerve lacerations at the forearm: an outcome study using RosénLundborg protocol. Microsurgery. 2011;31:253-262.
25.
Shaw AD, Milne AA, Christie J, Jenkins AM, Murie JA, Ruckley C V. Vascular trauma of the upper limb and associated nerve injuries. Injury. 1995;26:515-518.
26.
Shi L. The delayed management of main arterial injuries in extremity trauma: Surgical challenges and outcomes. Pakistan J Med Sci. 2013;29:64-67.
27.
Kline DG, Judice DJ. Operative management of selected brachial plexus lesions. J Neurosurg. 2009;58:631-649.
28.
Iriz E, Kolbakir F, Sarac A, Akar H, Keçeligil HT, Demirag MK. Retrospective assessment of vascular injuries: 23 years of experience. Ann Thorac Cardiovasc Surg. 2004;10:373-378.
29.
Eser F, Aktekin L, Bodur H, Atan C. Etiological factors of traumatic peripheral nerve injuries. Neurol India. 2009; 57:434-437.
TBPI Vascular 19 30.
Manord JD, Garrard CL, Kline DG, et al. Management of severe proximal vascular and neural injury of the upper extremity. J Vasc Surg. 1998;27:43-49.
31.
Razmadze A. Vascular injuries of the limbs: A fifteen-year Georgian experience. Eur J Vasc Endovasc Surg. 1999;18:235-239.
32.
Sen RK, Prasad G, Aggarwal S. Scapulothoracic dissociation: level of vascular insult, an indirect prognostic indicator for the final outcome? Acta Orthop Belg. 2009;75:14-18.
33.
Brucker PU, Gruen GS, Kaufmann RA. Scapulothoracic dissociation: evaluation and management. Injury. 2005;36:1147-1155.
34.
Damschen DD, Cogbill TH, Siegel MJ. Scapulothoracic dissociation caused by blunt trauma. J Trauma - Inj Infect Crit Care. 1997;42:537-540.
35.
Masmejean EH, Asfazadourian H, Alnot JY. Brachial plexus injuries in scapulothoracic dissociation. J Hand Surg Am. 2000;25:336-340.
36.
Riess KP, Cogbill TH, Patel NY, Lambert PJ, Mathiason MA. Brachial plexus injury: Long-term functional outcome is determined by associated scapulothoracic dissociation. J Trauma - Inj Infect Crit Care. 2007;63:1021-1025.
37.
Campbell WW. Evaluation and management of peripheral nerve injury. Clin Neurophysiol. 2008;119:1951-1965.
38.
Kline DG, Kim D, Midha R, Harsh C, Tiel R. Management and results of sciatic nerve injuries: a 24-year experience. J Neurosurg. 1998;89:13-23.
39.
Merrell GA, Barrie KA, Katz DL, Wolfe SW. Results of nerve transfer techniques for restoration of shoulder and elbow function in the context of a meta-analysis of the English literature. J Hand Surg Am. 2001;26:303-314.
40.
Secer HI, Daneyemez M, Gonul E, Izci Y. Surgical repair of ulnar nerve lesions caused
TBPI Vascular 20 by gunshot and shrapnel: results in 407 lesions. J Neurosurg. 2007;107:776-783. 41.
Pannell WC, Heckmann N, Alluri RK, Sivasundaram L, Stevanovic M, Ghiassi A. Predictors of Nerve Injury After Gunshot Wounds to the Upper Extremity. Hand. 2017;12:501-506.
42.
Selecki BR, Ring IT, Simpson DA, Vanderfield GK, Sewell MF. Trauma to the central and peripheral nervous systems. Part II: A statistical profile of surgical treatment New South Wales 1977. Aust N Z J Surg. 1982;52:111-116.
43.
Rich N, Spencer F. Vascular Trauma. Philadelphia: WB Saunders Co; 1978.
44.
Visser PA, Hermreck AS, Pierce GE, Thomas JH, Hardin CA. Prognosis of nerve injuries incurred during acute trauma to peripheral arteries. Am J Surg. 1980;140:596-599.
45.
Ballard JL, Bunt TJ, Malone JM. Management of small artery vascular trauma. Am J Surg. 1992;164:316-319.
46.
Brown PW. Factors influencing the success of the surgical repair of peripheral nerves. Surg Clin North Am. 1972;52:1137-1155.
47.
Kline DG, Hackett ER. Reappraisal of timing for exploration of civilian peripheral nerve injuries. Surgery. 1975;78:54-65.
48.
Suzuki K, Doi K, Hattori Y, Pagsaligan JM. Long-term results of spinal accessory nerve transfer to the suprascapular nerve in upper-type paralysis of brachial plexus injury. J Reconstr Microsurg. 2007;23:295-299.
49.
Elhassan B, Bishop AT, Hartzler RU, Shin AY, Spinner RJ. Tendon transfer options about the shoulder in patients with brachial plexus injury. J Bone Jt Surg - Ser A. 2012;94:1391-1398.
Table 1. British Medical Research Council Grade 48 Grade
Description
0
No contraction
1
Flicker or trace contraction
2
Active movement with gravity eliminated
3
Active movement against gravity
4
Active movement against gravity and resistance
5
Normal power
Table 10. DASH and VAS Scores Score, median (range)
Control
Vascular
p-value
Pre-op DASH
45.0 (1.7-90.8)
45.0 (10-94.2)
0.47
Post-op DASH
31.7 (0-91.7)
28.8 (0-71.7)
0.59
Pre- to post-op delta DASH
-13.4 (-60.8-68.4)
-15.0 (-58.3-20)
0.17
Pre-op VAS
3.2 (0-10)
4.4 (0-10)
0.38
Post-op VAS
2.3 (0-10)
2.0 (0-10)
0.63
Pre- to post-op delta VAS
-0.3 (-6.4-4.2)
-0.95 (-8.4-5.3)
0.14
Table 11. Elbow Flexion, BMRC Grade Grade
Pre-operative (n,%)
Post-operative (n,%)
Control
Vascular
Control
Vascular
0
85 (77)
25 (89)
6 (5.4)
8 (29)
1
4 (3.6)
2 (7.1)
7 (6.3)
3 (11)
2
7 (6.3)
0 (0)
18 (16)
5 (18)
3
3 (2.7)
1 (3.6)
23 (21)
6 (21)
4
2 (1.8)
0 (0)
33 (30)
5 (18)
4+
10 (9)
0 (0)
24 (22)
1 (3.6)
p-value
0.31
0.003
Table 12. Shoulder Abduction, BMRC Grade Grade
Pre-operative (n,%)
Post-operative (n,%)
Control
Vascular
Control
Vascular
0
79 (71)
18 (64)
23 (21)
9 (32)
1
8 (7.2)
1 (3.6)
15 (14)
3 (11)
2
8 (7.2)
3 (11)
27 (24)
7 (25)
3
8 (7.2)
3 (11)
25 (22)
3 (11)
4
5 (4.5)
2 (7.1)
12 (11)
3 (11)
4+
3 (2.7)
1 (3.6)
9 (8.1)
3 (11)
p-value
0.89
0.68
Table 13. Shoulder External Rotation, BMRC Grade Grade
Pre-operative (n,%)
Post-operative (n,%)
Control
Vascular
Control
Vascular
0
86 (77)
22 (79)
48 (43)
16 (57)
1
7 (6.3)
1 (3.6)
18 (16)
3 (11)
2
4 (3.6)
2 (7.1)
18 (16)
3 (11)
3
6 (5.4)
1 (3.6)
9 (8.1)
1 (3.5)
4
5 (4.5)
1 (3.6)
10 (9.0)
2 (7.1)
4+
3 (2.7)
1 (3.6)
8 (7.2)
3 (11)
p-value
0.95
0.71
Table 14. Pre-Operative, Post-Operative, and Change in Range of Motion (ROM) Control
Vascular
p-value
Pre/Post/Delta
Pre/Post/Delta
Pre/Post/Delta
Elbow flexion
18/96/77
3.2/54/51
0.11/0.003/0.07
Elbow extension
0/1.4/1.4
0/1.8/1.8
NA*/0.84/0.84
Shoulder external rotation
6.8/15/8.5
9.6/15/5.0
0.56/0.91/0.40
Shoulder abduction
13/47/33
19/36/17
0.58/0.38/0.12
Shoulder extension
3.4/9.6/6.2
4.6/8.9/4.3
0.63/0.87/0.54
Shoulder forward flexion
14/48/34
20/37/17
0.47/0.39/0.11
Mean ROM (degrees)
*all patients demonstrated 0 degrees of elbow extension pre-operatively. Abbreviations: pre = pre-operative; post = post-operative; delta = change between pre- and post-operative
Table 2. Classification of Scapulothoracic Dissociation17 Type 1
Description Isolated musculoskeletal injury
2A
Musculoskeletal and vascular injury
2B
Musculoskeletal and incomplete neurologic injury
3
Musculoskeletal, vascular, and incomplete neurologic
4
Musculoskeletal injury, vascular, and complete brachial plexus avulsion
Table 3. Patient Demographics Characteristic
Control
Vascular
p-value
Age, median (range)
31 (16-69)
28 (16-68)
0.11
Gender F/M, N (%)
37 (14) / 220 (86)
7 (12) / 61 (88)
0.43
Follow-up duration (months), median (range)
25.2 (0-188.3)
25.0 (0-152.6)
0.96
Table 4. Etiology of Injury Etiology
Control (n, %)
Vascular (n,%)
p-value
Laceration
2 (1)
2 (3)
0.19
GSW
2 (1)
2 (3)
0.19
MVA
214 (83)
60 (88)
0.36
Fall from height
15 (6)
0 (0)
0.05
Other
24 (9)
4 (6)
0.36
Table 5. Level of AT-BPI Level
Control (n,%)
Vascular (n,%)
p-value
Upper trunk only
71 (28)
1 (1)
<0.0001
Upper trunk + C7 only
58 (23)
4 (6)
0.0003
Pan-plexus
128 (50)
63 (93)
<0.0001
Table 6. Associated Ipsilateral Injuries Location
Control (n,%)
Vascular (n,%)
p-value
Thoracic cavity injury
83 (32)
22 (47)
1.00
Rib fractures
71 (28)
11 (16)
0.06
Pneumothorax
36 (14)
12 (18)
0.45
Shoulder girdle injury
88 (34)
21 (30)
0.67
Clavicle fracture
58 (23)
11 (16)
0.25
Scapular fracture
37 (14)
11 (16)
0.71
Spinal fracture
63 (25)
16 (24)
1.00
UE injury
83 (32)
42 (62)
<0.0001
Humeral fracture
27 (11)
16 (24)
0.008
Radial fracture
26 (10)
18 (26)
0.001
Ulnar fracture
18 (7)
16 (24)
0.0003
Wrist or hand injury
24 (9)
5 (7)
0.81
LE injury
52 (20)
14 (26)
1.00
No ipsilateral injuries
65 (25)
8 (12)
0.02
Table 7. Presence of Scapulothoracic Dissociation Group
N (% of group)
Zelle 2B
Zelle 3
Zelle 4
Control
10 (3.9)
7
0
3
Vascular
5 (7.4)
0
4
1
Table 8. Type of Nerve Reconstruction Procedure
Control
Vascular
p-value
Direct nerve repair
2 (0.8)
1 (1.5)
0.36
Nerve graft
121 (47)
54 (79)
0.003
Nerve transfer
181 (70)
31 (46)
0.002
FFMT
56 (22)
7 (10)
0.21
Table 9. Type of Vascular Reconstruction Procedure
N (% of vascular group)
Primary arterial repair
10 (15)
Vessel graft
43 (63)
Vessel stent
7 (10)
Vessel bypass
16 (23)
Vessel ligation
3 (4)
No repair performed
4 (6)
Alice Huang contributed to the conception, execution of the
study, data collection, analysis and interpretation of the data and drafting the manuscript for submission. Shelley Noland contributed to the conception and interpretation
of data, the acquisition of funding and editing the manuscript. Robert Spinner contributed to the conception and interpretation
of data, the acquisition of funding and editing the manuscript. Allen Bishop contributed to the conception and interpretation
of data, the acquisition of funding and editing the manuscript. Alexander Shin contributed to the conception and interpretation
of data, the acquisition of funding and editing the manuscript.
Abbreviations: adult traumatic brachial plexus injury (AT-BPI) nerve action potentials (NAP) somatosensory evoked potentials (SSEP) motor evoked potential (MEP) British Medical Research Council (BRMC) range of motion (ROM) Disability of Arm-Shoulder-Hand Questionnaire (DASH) free functioning muscle transfers (FFMT). Scapulothoracic dissociation (SD)