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Brachial Plexus Injury Management in Military Casualties: Who, What, When, Why, and How Li Col James A. Chambers, USAF MC*; Capt Claire L. Hiles, USAF MCf; CPT Brian P. Keene, MC USAf ABSTRACT The Global War on Terrorism has achieved an unprecedented 90% casualty survival rate because of far forward surgical support, rapid transport, and body armor. Despite the reinarkable protection body armor affords, peripheral nerve injuries continue to occur. The brachial plexus in particular is still susceptible to penetrating trauma through the axilla as well as blunt mechanisms. We report 1,818 individuals with reported cases of peripheral nerve injury, 97 of which had brachial plexus itijury incident from Operation Iraqi Freedom and Operation Enduring Freedom. We suspect that true prevalence is higher as initial focus on vascular and orthopedic reconstruction in complex shoulder injuries may overlook brachial plexus lesions. Accordingly, emergency physicians, general and orthopedic trauma surgeons, and vascular surgeons should all consider the possibility of brachial plexus and other peripheral nerve injury for early and appropriate referral to surgeons (plastic, orthopedic, or neurosurgical) for further evaluation and reconstruction. The latter group should be familiar with appropriate modem diagnostic and initial as well as salvage therapeutic options.

Injuries to the brachial plexus with subsequent paralysis of the upper extremity are as old as warfare. Homer, in his Iliad, and Thucydides, in his History of the Peloponnesian War, eloquently described the devastating nature of direct or indirect injury to the upper extremity, witii injured chariot drivers constituting the patient population at the time. War, unfortunately, and other events resulting in injuries have stimulated the studying of this clinical entity, even in the modern era. Terzis John

INTRODUCTION As mortality rates declined from 30% to 10% from World War II to the Global War on Terrorism, respectively, military medicine shifted focus to treating service members who survived combated-related wounds, especially complex injuries of the upper and lower extremities.'" Brachial plexus injuries are among these injuries, resultant of often devastating lesions in young, otherwise healthy individuals, potentially robbing them of optimal productivity and fulfillment. In civilians, blunt trauma from motorcycle or automobile accidents account for the majority of cases.'' Limited data has been published on the incidence, prevalence, and treatment of injuries to peripheral nerves, such as the brachial plexus, in recent military conflicts. A recent analysis by »Office of the Air Force Surgeon General, AFMSA/SG3XI, 7700 Arlington Boulevard. Suite 5156, Ealls Church, VA 22042. tDepartment of Internal Medicine, San Antonio Military Medical Center, 3551 Roger Brooke Drive, Fort Sam Houston, TX 78234. tLandstuhl Regional Medical Center, MEDCOM ERMC. Building 20, RM 51, Landstuhl/Kirchberg, Germany, 66849. The view(s) expressed herein are those of the author(s) and do not reflect the official policy or position of Brooke Army Medical Center, the U.S. Army Medical Department, the U.S. Army Office of the Surgeon General, the Department of the Air Force or Army, Department of Defense, or the U.S. Government. doi; 10.7205/MILMED-D-13-00457

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Brininger et al, comparing peacetime (1998-2001) to wartime years (2002-2006), noted an 89% increase in brachial plexus injuries across all service branches. Since the inception of the Global War on Terror in 2002, at least 97 cases of brachial plexus injury and 1,818 cases of any peripheral nerve injury have been reported in U.S. troops from Iraq and Afghanistan. Unlike their civilian counterparts, the majority of these cases resulted from penetrating injury on the battlefield. Given the relative infrequency of this condition compared with 47,232 total wounded in action,^ and the importance of appropriate early diagnosis, this article seeks to outline the appropriate evaluation and management. HISTORY Ancient Nearly 3,000 years ago. Homer recorded in The Iliad two instances of probable brachial plexus injuries sustained upon the battlefield of Troy.^ Eirst, when Hector strikes Teucer with a stone over his clavicle making him unable to wield his bow. " . . . [Hector] hit him just where the collar-bone divides the neck from the chest, a very deadly place, and broke the sinew of his arm so that his wrist was less, and the bow dropped from his hand as he fell forward on his knees." The second is when Achilles strikes Hector with his spear in the neck causing him to lose grip of his spear. " . . . [Achilles] eyed his [Hector's] fair flesh over and over to see where he could best wound it, but all was protected by the goodly armor of which Hector had spoiled Patroclus after he had slain him, save only the throat where the collar-bones divide the neck from the shoulders, and this is a most deadly place.. ."^ These passages from the Iliad demonstrate that the lateral cervical region of the neck, specifically the brachial plexus, was recognized as a vulnerable area because it was not protected by body armor and the injuries sustained were vastly devastating, if not fatal.

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Brachial Plexus Injury Management in Military Casualties

Early Civilian Even with the development of general anesthesia, general pessimism prevailed regarding brachial plexus surgery in the first half of the 20th century because of reports of high morbidity and mortality with disappointing results.**'^

Military World War II Multiple authors reported discouraging results in cases treated during World War II, asserting that surgical intervention was rarely justified."*'" The pioneering techniques of Sir Herbert Seddon in nerve grafting would have to wait for improvements in surgical instrumentation and optics to be more successfully developed.

Military After World War II Nelson et al reported 9 cases of brachial plexus trauma from chest missile wounds in Vietnam. Nelson et al illustrated a significant delay in the recognition of most brachial plexus injuries secondary to the need for immediate stabilization and evacuation of soldiers for high-energy combat woutids, and relative infrequency of brachial plexus injuries. Stating that "surgical exploration to afford anatomic display of the brachial plexus ... is not justified when the reestablishment of cardiorespiratory stability becomes a primary consideration."'^ For treatment, the study recommends "conservative management" with physical therapy or neurolysis in those with more severe injuries.

Civilian After World War II Millesi • and numerous other surgeons capitalized upon advances in diagnostic and therapeutic technological advances and refined techniques for modem application.

Modern Non-U.S. Conflicts Ghahremani"* reported managing 71 cases of brachial plexus injuries from the Iran-Iraq War (1980-1988). Of these, 80% of the cases were from shell fragments, resulting in a significant (30%) coincidence of vascular injury. Only 20% of cases involved root avulsion, and over half (55%) were injured at the level of the cords. A combination of nerve transfers, free vascular nerve grafting, and cable grafting were used with variable success. Four cases of blunt injury from shock waves were reported, two of which required surgery in the form of neurolysis.'^ Gousheh also reported his experience during the same conflict with 369 brachial plexus injuries, 246 of whom had >5 years follow-up. Similar to Ghahremani's experience, 90% of the injuries were from shell fragments, with over half involving the cords and terminal branches. Only 11% over Gousheh's patients, however, had concomitant vascular injury. The author noted that "most of the complicated plexus injuries were associated with comminuted fractures or shattered bones."'^

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Operation Enduring Freedom/Operation Iraqi Freedom In review of the Joint Theater Trauma Registry, there are 97 reported cases of brachial plexus injury from Operation Iraqi Freedom and Operation Enduring Freedom. Typical of most armed conflicts, the majority of cases (73 cases) were from penetrating trauma, whereas 23 cases were secondary to blunt trauma. These required immediate surgical exploration for damage control and re-exploration for definitive treatment once evacuated from theater. ANATOMY The brachial plexus begins as five spinal cord roots, C5:T1, which contributes to three trunks (superior, middle, and inferior). The trunks further divide into cords that split into six branches (anterior/posterior segments of superior, middle, and inferior trunks). The cords are named according to their relation to the axillary artery (medial, lateral, and posterior). The six postclavicular branches then compose the musculocutaneous, median, ulnar, axillary, radial, and thoracodorsal nerves. The four preclavicular branches make up the dorsal scapular, suprascapular, long thoracic, and nerve to subclavius. The terminal muscle groups supplied by these branches are easily evaluated by physical examination.'^ CLASSIFICATION The Seddon and Sunderland types and classification of nerve injuries are the most commonly used to describe peripheral nerve injury. The Seddon classification system involves three types of injury spanning from "neuropraxia," a temporary loss of function with spontaneous full recovery from symptoms, to "axonotmesis" or nerve damage with partial recovery from symptoms, and "neurotmesis," a permanent nerve lesion with complete loss of function without surgical intervention. The Sunderland classification involves five degrees of injury with a first-degree injury resulting in transient loss of function and a fifth degree resulting in permanent loss of function. A first-degree injury is equivalent to neuropraxia. Injury of the second degree is equivalent to axonotmesis. Third-degree injury involves damage to the endoneurium, with the possibility of functional recovei-y. A fourth-degree injury results when all areas of the nerve are injured, with preservation of the epineurium. A recovery is possible with surgical intervention. Fifth-degree injury is similar to the fourth-degree injury, but the epineurium is no longer intact.'^ EVALUATION

History A detailed clinical history provides the foundation for evaluation. Loss of consciousness, mechanism of injury, wearing of any protective equipment, associated snapping, popping.

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locking, tightness, or crepitation, and other relevant details should be recorded. History of prior injury or surgeries to the neck and peripheral nerves effects projected prognosis as well as may alter options of repair. If Homer syndrome is encountered, a detailed ophthalmic history should be obtained as well.

Physical Advanced Trauma Life Support protocols must be adhered to as with any trauma patient. Adequate neurologic assessment may be delayed because of sedation; however, associated injuries must be suspected and ruled out. Vascular lesions in particular merit attention because of frequency and significance. Although, emphasis on the injured extremity is appropriate, additional findings elsewhere such as Homer's syndrome should be sought and documented. Palpation of the cervical spine should occur first to rule out a neck injury, Musculoskeletal examination should include passive and active range of motion of the neck and both extremities, bilateral strength, sensation by nerve domain (soft touch, pain, static, and two-point discrimination), and evidence of prior rib fracture may be important for possible use of intercostal nerves for harvest. Neurological examination should include examination of cranial nerve XI, stemocleidomastoid, and trapezius. Several suggestive signs and symptoms of neural disruption include numbness or buming of the entire arm, hand, and fingers, sensory loss over a dermatomal distribution, complete transient paralysis of the affected nerves, and tendemess over the brachial plexus."* Vascular examination with palpation, doppler, and when clinically suspected (bruit, consideration for flap surgery), angiography is appropriate. Signs suggestive of a root avulsion are particularly itnportant. A positive supraclavicular Tinel's sign (tingling noted in the affected extremity) suggests rupture, rather than avulsion."^ An ipsilateral Homer's sign (eyelid ptosis, miosis, and anhydrosis), conversely, is associated with root avulsion.

Radiographic Plain films should be obtained to evaluate the cervical spine, clavicle, and scapula. Inspiratory and expiratory chest radiograph should be examined for elevated hemidiaphragm suggesting phrenic nei"ve injury, and fractured ribs may indicate damage to intercostal nerves, which otherwise could be used for neurotization. Computed tomography myelography has been found to have particular sensitivity in detecting pseudomeningoceles, which are strongly associated with root avulsion. In one study, this modality demonstrated 95% sensitivity and 98% specificity for avulsion.'^ One month should pass after injury before obtaining computed tomography myelography to optimize sensitivity,^ and only in those patients in whom surgical intervention is being considered.

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Electrophysiological Resting and active electromyography (EMG) and nerve conduction studies are ideally performed from 3 to 6 weeks after injury allowing for evidence of Wallerian degeneration to manifest. The first test serves as a baseline for serial testing, usually performed monthly for evaluation of electrophysiological recovery. Motor function is recorded in addition to presence of fibrillation potentials at rest and with voluntary movement. Sensory nerve action potentials are normal in lesions proximal to the dorsal root ganglion, however, absent in postganglionic or combined lesions.^" Intraoperatively, it is recommended that paralytic agents are avoided, and sedation with sufentanil be utilized so that nerve action potentials (NAPs) can be measured. Preservation of NAPs suggests intact axons or axonal regeneration. According to Tiel et al,"^' "90% of patients with preserved NAP will gain clinically useful recovery." Somatosensory-evoked potentials may increase in response to peripheral stimulation if there is "continuity between the peripheral nervous system and the central nervous system via a dorsal root." However, somatosensory-evoked potentials are absent in postgangliotiic or combined lesions as with sensory nerve action potentials.20 TREATMENT We have developed a functional algorithm for early and long-term management options following rapid identification of brachial plexus injuries (Fig. 1). Through identification of particular types of injuries, initial providers may utilize such an algorithm to appropriately and swiftly refer surgical cases for early repair as well as work to prevent further injury. Time is the critical factor in the evaluation and treatment of these injuries as recovery is time-dependent. Irreparable neuromuscular loss occurs 12 to 18 months after injury.^^ Immediate surgical exploration is indicated for penetrating injuries associated with vascular and skeletal trauma, or complicated by limb ischemia. Early exploration (3 weeks3 months) is indicated for total palsy or high-energy injury. When there is evidence of incomplete lesion, a period of observation is warranted as these injuries tend to do better without surgery. However, if there is no improvement of Tinel's sign or recovery plateaus, late exploration at 3 to 6 months is indicated. Even with surgery, the recovery process for a peripheral nerve injury is often lengthy in duration from 6 to 18 months and often incomplete. Nonsurgical early management should focus on pain control and prevention of further injury immediately following injury with early physical therapy and limited immobilization to prevent debilitating joint contractures. Long-term rehabilitation may include physiotherapy, occupational therapy, physical therapy, and electrical stimulation.

Direct Repair Direct nerve repair, or primary nerve repair, is the repairing of a sharply transected nerve using microscopic neurosurgical

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Brachial Plexus Injury Blutit Injury Immediate Surgery -Indicated for total palsy Early Surgery (3 wks to 3 months) - For persistence of symptoms - EMG without evidence of recovery Late Surgery (3-6 months) - Persistence of symptoms - Failure to progress by EMG

Penetrating/Crush Injury Prevent Further Injury Immediately after injury - Early Physical Therapy - Limit immobilization to 2 weeks EMG @ 3-6 weeks - To allow for Wallerian Degeneration - Then monthly to evaluate for electrophysiological recovery

Immediate Surgical Exploration - Neurolysis - Intraoperative Nerve Testing - Primary vs Delayed Repair - Bank Nerve Grafts for delayed repairs - Nerve transfers

t2 months from time of injury - Salvage procedures -Consider Functional Free muscle or tendon transfers, bone blocks, or rotational osteotomies.

FIGURE 1.

Brachial plexus injury algorithm.

techniques atid sufures, with or without fibriti glue. This is the optitnal method of treatment when the expected time of nerve regeneration does not exceed the remaining time before in-eparable loss. Injuries that are very proximal are not amenable to direct repair.

biceps. In selection of appropriate donor nerve for transfer, the most important criteria are expendability and proximity to the recipient end organ. Spinal accessory nerve to supraspinatus transfer, or a dual nerve transfer to the suprascapular and axillary nerve showed good results for restoration of shoulder abduction.

Nerve Graft Nerve grafting requires a viable motor axon, or intetpositional nerve graft that is used to connect two points of peripheral nerve, with the possibility of regeneration of function over time. This method rnay be sought when a gap exists and both intact nerve ends cannot be mobilized enough to allow a tension-free repair. Sural nerve, a minimum of 5 bundles, was often grafted to repair multiple trunk and cord level lesions with overall good results to the lateral, medial, and posterior cord. Gousheh reported 87.1% of patients experienced "good" digital flexion, but with a 29,7% failure rate for finger extension. For terminal branches, (median, radial, ulnar, musculocutaneous, and axillary), they reported 85.1% good results with a 5.7% failure rate.'^

Nerve Transfer Nerve transfer is the process by which a nerve of lesser function is sacrificed to achieve an improvement in overall functional status for the patient. This method offers the distinct advantages over primary nerve repair in that transfer may be performed much closer to the end organ and thus require less time for reinnervation.^' Merrell et aP^ describe excellent results with intercostal to musculocutaneous transfers achieving 72% muscle strength 3/5 or greater of the

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Muscle/Tendon Transfer Latissimus dorsi, pectoralis, or rectus femoris muscles can be reconstructed to provide elbow flexion.'^ Steindler flexorplasty is indicated no sooner than 12 months after nerve transfer for muscle strength less than 3/5. In the Steindler technique, the insertion of the pronator mass is moved proximally on the humérus to aid with elbow flexion.""* Doi^"'' describes a double-free muscle transfer using gracillis muscle to restore hand function.

Future Treatment Options Low-level laser phototherapy is currently in trials for treatment of peripheral nerve injury. It is intended to enhance and accelerate the healing process in patients after peripheral nerve surgery and/or following traumatic injury. Preliminary results from a small randomized, controlled, double-blind pilot study by Rochkind et aP*" demonstrated significant improvement in the recruitment of voluntaiy muscle activity in the laser-treated group (p = 0.006) compared to the placebo group. This method looks to offer a safe, noninvasive, and easy to implement therapy to return limb and motor function to a more complete state.

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SUMMARY There should be a high index of suspicion for brachial plexus injury following traumatic injury to the upper extremity. Often times there are delays in treatrnent because of immediate stabilization and immobilization. Brachial plexus injuries should be immobilized for the shortest time period possible and physical therapy should be started early. Early referral to high-volume centers should be initiated to optimize management and surgical treatment options. EMG studies should be conducted at minimum of 3 weeks after the injury to evaluate for fibrillations, and then every 3 to 4 weeks following. Immediate surgical exploration indicated for total palsies or penetrating traumatic injuries with delayed surgery for persistent symptoms or plateau in recovery. Late surgery and palliative surgery is indicated at 6 to 12 months for failure of neurolysis, direct repairs, and nerve transfers. REFERENCES 1. Gawande A: Casualties of war—military care for the wounded from Iraq and Afghanistan. N Engl J Med. 2004; 351(24): 2471-5. 2. Department of Defense: Principal wars in which the United States participated: U.S. military personnel serving and casualties 2007. Available at http://webl.whs.osd.mil/mmid/casualty/WCPRINCIPAL; accessed July 28, 2007. 3. Terzis J, Papakonstantinou K: The surgical treatment of brachial plexus injuries in adults, Plast Reconstr Surg 2000; 106(5): 1097-122. 4. Brininger TL, Antczak A, Breland HL: Upper extremity injuries in ihe U.S. military during peacetime years and wartime years. J Hand Ther 2008; 21(2): 115-22. 5. Department of Defense: Operation Iraqi Freedom & Operation Enduring Freedom U.S. Casualty Status 2012. Available at http://www.defense.gov/ news/casualty.pdf: accessed February 2, 2012. 6. Aydin A, Tumerdem B, Yazar M. Erer M: Three-thousand-year-old written reference to a description of what might be the earliest brachial plexus injuries in the Iliad of Homer. Plast Reconstr Surg 2004; 114(5): 1352-3. 7 Homer: The Iliad. Available at http://www.Iiteraturepage.com; accessed October 15, 2013. 8 Clark L, Taylor A, Prout T: Study on brachial plexus birth palsy. Am JMed Sei 1905; 130: 670-9. 9. Taylor A: Brachial birth palsy and injuries of similar type in adults. Surg Gynecol Obstet 1920; 30: 494-502.

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10. Nulsen F, Slade H: Recovery Following Injuries to the Brachial Plexus. Washington. DC. U.S. Government Printing Office, 1956. 11. Brooks DM: Open wounds of the brachial plexus. J Bone Joint Surg Br 1949; 31B(1): 17-33. 12. Nelson KG, Jolly PC, Thomas PA: Brachial plexus injuries associated with missile wounds of the chest: report of 9 cases from Viet Nam. J Trauma 1968; 8(2): 268-75. 13. Millesi H: Microsurgery of peripheral nerves. Hand 1973; 5(2): 157-60. 14. Ghahremani S: Brachial plexus injury in war victims. J Hand Surg Am 2003; 28B (Supp 1): 9. 15. Gousheh J: The treatment of war injuries of the brachial plexus. J Hand Surg Am 1995; 20A(3): S68-76. 16. Beredjiklian PK, Bozentka DJ: Review of Hand Surgery, Ed 1, Philadelphia, Saunders, 2004. 17. Burnett MG, Zager EL: Pathophysiology of peripheral nerve injury: a brief review: nerve injury classification. Neurosurg Focus 2004; 16(5): El. 18. Haynes S: Systematic evaluation of brachial plexus injuries. J Athl Train 1993; 28(3): 263-7. 19. Walker AT, Chaloupka JC, deLotbiniere AC, Wolfe SW, Goldman R, Kier EL: Detection of nerve rootlet avulsion on CT myelography in patients with birth palsy and brachial plexus injury after trauma. AJR Am J Roentgenol 1996; 167(5): 1283-7. 20. Shin AY. Spinner RJ, Steinmann SP, Bishop AT: Adult traumatic brachial plexus injuries. J Am Acad Orthop Surg 2005; 13(6): 382-96. 21. Tiel RL, Happel LT Jr.. Kline DG: Nerve action potential recording method and equipment. Neurosurgery 1996; 103(8): 108—9. 22. Mackinnon S, Colbert S: Nerve transfers in the hand and upper extremity surgery. Tech Hand Up Extrem Surg 2008; 12(1): 20-33, 23. 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; 26A(2): 303-14, 24. Teboul F, Kakkar R, Ameur N, Beaulieu J, Oberlin C: Transfer of fasicles from the ulnar nerve to the biceps in the treatment of upper brachial plexus palsy. J Bone Joint Surg Am 2004; 86A(7): 1485-90. 25. Doi K: Restoration of prehension with the double free muscle technique following complete avulsion of the brachial plexu.s. Indications and long-term results. J Bone Joint Surg Am 2000; 82A: 652. 26. Rochkind S, Drory V, Alón M, Nissan M, Ouaknine G: Laser phototherapy (780 nm), a new modality in treatment of long-term incomplete peripheral nerve injury: a randomized double-blind placebo-controlled study. Photomed Laser Surg 2007; 25(5): 436-42.

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Brachial plexus injury management in military casualties: who, what, when, why, and how.

The Global War on Terrorism has achieved an unprecedented 90% casualty survival rate because of far forward surgical support, rapid transport, and bod...
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