Nerve transfers for the restoration of hand function after spinal cord injury

Case report

Restricted access

Spinal cord injury (SCI) remains a significant public health problem. Despite advances in understanding of the pathophysiological processes of acute and chronic SCI, corresponding advances in translational applications have lagged behind. Nerve transfers using an expendable nearby motor nerve to reinnervate a denervated nerve have resulted in more rapid and improved functional recovery than traditional nerve graft reconstructions following a peripheral nerve injury. The authors present a single case of restoration of some hand function following a complete cervical SCI utilizing nerve transfers.

Abbreviations used in this paper:AIN = anterior interosseous nerve; ASIA = American Spinal Injury Association; ICSHT = International Classification for Surgery of the Hand in Tetraplegia; MRC = Medical Research Council; SCI = spinal cord injury.

Article Information

Address correspondence to: Wilson Z. Ray, M.D., Department of Neurological Surgery, Washington University School of Medicine, 660 South Euclid Avenue, St. Louis, Missouri 63110. email: rayz@wudosis.wustl.edu.

Please include this information when citing this paper: published online May 15, 2012; DOI: 10.3171/2012.3.JNS12328.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Preoperative physical examination of the left and right upper extremities. A–E: Left upper extremity. The patient exhibited strong elbow flexion (A), strong pronation (B), strong wrist flexion (C), strong wrist extension (D), but no finger or thumb movement (E). F–J: Right upper extremity. The patient exhibited strong elbow flexion (F) and his pronation was near normal in strength (slight weakness)(G). He was able to flex his wrist, but not against resistance specifically testing flexor carpi radialis (H). His wrist extension was strong with slight weakness in wrist extension (I). He exhibited no finger or thumb movement (J).

  • View in gallery

    Musculocutaneous and median nerve anatomy relevant to the brachialis nerve to AIN transfer in C-7 SCI. A: The donor brachialis branch divides from the musculocutaneous nerve on its medial aspect. After this branch point, the musculocutaneous nerve becomes the lateral antebrachial cutaneous nerve. B: The recipient AIN branches from the median nerve in the forearm on its lateral aspect, but courses proximally into the arm on its posterior/medial aspect. The donor brachialis nerve is transferred into the anterior interosseous fascicle in the arm. C: The AIN fascicle in the arm is located on the posterior/medial aspect of the median nerve, between the palmaris longus/flexor digitorum superficialis/flexor carpi radialis fascicle and the sensory component of the median nerve. The fascicular group to the pronator teres is located in the anterior portion of the median nerve, while the sensory fibers are lateral and the motor fibers medial. A = anterior; L = lateral; M = medial; N = nerve; P = posterior; R = radial; U = ulnar.

  • View in gallery

    Intraoperative electrical stimulation of the nonintact nerves. A: Stimulation of the right anterior interosseous fascicle with the hand at rest and contraction of the flexor pollicis longus and median nerve–innervated flexor digitorum profundus. B: Stimulation of the right ulnar nerve with the hand at rest and contraction of the intrinsic muscles, more apparent on the lateral aspect. C: Stimulation of the left anterior interosseous fascicle with the hand at rest and contraction. The blue arrows indicate change from the nonstimulated to the stimulated condition.

  • View in gallery

    Qualitative histological assessment of the brachialis nerve and AIN in the right extremity. Upper: A small fascicle of the brachialis nerve reveals normal myelinated nerve fibers. This fascicle is not representative of the brachialis branch used as the donor nerve for transfer. Lower: Assessment of the nonintact AIN reveals sporadic myelinated fibers. Original magnification × 100.

  • View in gallery

    Brachialis nerve–AIN transfer in the left upper extremity. A: The anterior interosseous fascicle was separated from the median nerve on its posterior/medial aspect. B: The distal branches of the brachialis nerve were identified. C: The brachialis nerve was transected distally and the anterior interosseous fascicle was separated proximally for transection. D: The donor brachialis nerve was transferred to the recipient anterior interosseous fascicle. LABC = lateral antebrachial cutaneous.

  • View in gallery

    Brachialis nerve–AIN transfer in the right extremity. A: The AIN was identified distally and followed proximally to identify its fascicular component. B: The distal branches of the brachialis nerve were identified. C: The brachialis nerve was transected distally and the anterior interosseous fascicle was separated proximally. D: The donor brachialis nerve was transferred to the recipient anterior interosseous fascicle.

  • View in gallery

    Postoperative examination of the left and right hands following brachialis nerve–AIN transfer. A and B: Left and right hands in resting position. C and D: Left and right hands performing AIN function through pinch with simultaneous activation of the donor brachialis nerve through elbow flexion. E and F: Functional recovery included the ability to grasp small objects such as a ball. G and H: The patient has recovered the ability to feed himself.

  • View in gallery

    Mirror therapy utilizing the left hand to rehabilitate the weaker right hand. Left: The patient used the left hand, with its recovered AIN function, to visualize the mirror image as the right hand during cocontraction. Right: The right hand within the mirror box.

References

1

Ackery ATator CKrassioukov A: A global perspective on spinal cord injury epidemiology. J Neurotrauma 21:135513702004

2

Bagriyanik HAOzogul CAlaygut EGokmen NKucukguclu SGunerli A: Neuroprotective effects of ketorolac tromethamine after spinal cord injury in rats: an ultrastructural study. Adv Ther 25:1521582008

3

Bao FLiu D: Peroxynitrite generated in the rat spinal cord induces neuron death and neurological deficits. Neuroscience 115:8398492002

4

Bertelli JAGhizoni MFTacca CP: Transfer of the teres minor motor branch for triceps reinnervation in tetraplegia. Case report. J Neurosurg 114:145714602011

5

Bertelli JATacca CPGhizoni MFKechele PRSantos MA: Transfer of supinator motor branches to the posterior interosseous nerve to reconstruct thumb and finger extension in tetraplegia: case report. J Hand Surg Am 35:164716512010

6

Brandt KEMackinnon SE: A technique for maximizing biceps recovery in brachial plexus reconstruction. J Hand Surg Am 18:7267331993

7

Brown JMMackinnon SE: Nerve transfers in the forearm and hand. Hand Clin 24:319340v2008

8

Brown JMShah MNMackinnon SE: Distal nerve transfers: a biology-based rationale. Neurosurg Focus 26:2E122009

9

Brunelli G: Research on the possibility of overcoming traumatic paraplegia and its first clinical results. Curr Pharm Des 11:142114282005

10

Brunelli Gvon Wild K: Unsuspected plasticity of single neurons after connection of the corticospinal tract with peripheral nerves in spinal cord lesions. J Korean Neurosurg Soc 46:142009

11

Carlsen BTKircher MFSpinner RJBishop ATShin AY: Comparison of single versus double nerve transfers for elbow flexion after brachial plexus injury. Plast Reconstr Surg 127:2692762011

12

Carlson SLParrish MESpringer JEDoty KDossett L: Acute inflammatory response in spinal cord following impact injury. Exp Neurol 151:77881998

13

Carlstedt TAnand PHallin RMisra PVNorén GSeferlis T: Spinal nerve root repair and reimplantation of avulsed ventral roots into the spinal cord after brachial plexus injury. J Neurosurg 93:2 Suppl2372472000

14

Dai KRYu CTWu RSZhang XFYuan JXSun YH: Intercostal-lumbar-spinal nerve anastomoses for cord transection. A preliminary investigation. J Reconstr Microsurg 1:2232261985

15

Déry MARousseau GBenderdour MBeaumont E: Atorvastatin prevents early apoptosis after thoracic spinal cord contusion injury and promotes locomotion recovery. Neurosci Lett 453:73762009

16

Eng LFLee YL: Response of chemokine antagonists to inflammation in injured spinal cord. Neurochem Res 28:951002003

17

Fleming JCBao FChen YHamilton EFGonzalez-Lara LEFoster PJ: Timing and duration of anti–α4β1 integrin treatment after spinal cord injury: effect on therapeutic efficacy. Laboratory investigation. J Neurosurg Spine 11:5755872009

18

Fournier HDMercier PMenei P: Repair of avulsed ventral nerve roots by direct ventral intraspinal implantation after brachial plexus injury. Hand Clin 21:1091182005

19

Guízar-Sahagún GRodríguez-Balderas CAFranco-Bourland REMartínez-Cruz AGrijalva IIbarra A: Lack of neuroprotection with pharmacological pretreatment in a paradigm for anticipated spinal cord lesions. Spinal Cord 47:1561602009

20

Kale SSGlaus SWYee ANicoson MCHunter DAMackinnon SE: Reverse end-to-side nerve transfer: from animal model to clinical use. J Hand Surg Am 36:163116392011

21

Kang CEPoon PCTator CHShoichet MS: A new paradigm for local and sustained release of therapeutic molecules to the injured spinal cord for neuroprotection and tissue repair. Tissue Eng Part A 15:5956042009

22

Konya DLiao WLChoi HYu DWoodard MCNewton KM: Functional recovery in T13–L1 hemisected rats resulting from peripheral nerve rerouting: role of central neuroplasticity. Regen Med 3:3093272008

23

Kumar PAHassan KM: Cross-face nerve graft with freemuscle transfer for reanimation of the paralyzed face: a comparative study of the single-stage and two-stage procedures. Plast Reconstr Surg 109:4514642002

24

Lin HHou CChen A: Reconstructed bladder innervation above the level of spinal cord injury to produce urination by abdomen-to-bladder reflex contractions. Case report. J Neurosurg Spine 14:7998022011

25

Lin HHou CZhen X: Bypassing spinal cord injury: surgical reconstruction of afferent and efferent pathways to the urinary bladder after conus medullaris injury in a rat model. J Reconstr Microsurg 24:5755812008

26

Liu SPeulve PJin OBoisset NTiollier JSaid G: Axonal regrowth through collagen tubes bridging the spinal cord to nerve roots. J Neurosci Res 49:4254321997

27

Livshits ACatz AFolman YWitz MLivshits VBaskov A: Reinnervation of the neurogenic bladder in the late period of the spinal cord trauma. Spinal Cord 42:2112172004

28

López-Vales RGarcía-Alías GForés JUdina EGold BGNavarro X: FK 506 reduces tissue damage and prevents functional deficit after spinal cord injury in the rat. J Neurosci Res 81:8278362005

29

López-Vales RRedensek ASkinner TARathore KIGhasemlou NWojewodka G: Fenretinide promotes functional recovery and tissue protection after spinal cord contusion injury in mice. J Neurosci 30:322032262010

30

Louie GMackinnon SEDellon ALPatterson GAHunter DA: Medial antebrachial cutaneous—lateral femoral cutaneous neurotization in restoration of sensation to pressure-bearing areas in a paraplegic: a four-year follow-up. Ann Plast Surg 19:5725761987

31

Mackinnon SEDellon ALPatterson GAGruss JS: Medial antebrachial cutaneous-lateral femoral cutaneous neurotization to provide sensation to pressure-bearing areas in the paraplegic patient. Ann Plast Surg 14:5415441985

32

Mackinnon SENovak CB: Nerve transfers. New options for reconstruction following nerve injury. Hand Clin 15:643666ix1999

33

Malik HGBuhr AJ: Intercostal nerve transfer to lumbar nerve roots. Part I: development of an animal model and cadaver studies. Spine (Phila Pa 1976) 4:4104151979

34

Mann CLee JHLiu JStammers AMSohn HMTetzlaff W: Delayed treatment of spinal cord injury with erythropoietin or darbepoetin—a lack of neuroprotective efficacy in a contusion model of cord injury. Exp Neurol 211:34402008

35

Matis GKBirbilis TA: Erythropoietin in spinal cord injury. Eur Spine J 18:3143232009

36

McDowell CLMoberg EAHouse JH: The Second International Conference on Surgical Rehabilitation of the Upper Limb in Tetraplegia (Quadriplegia). J Hand Surg Am 11:6046081986

37

McTigue DMTripathi RWei PLash AT: The PPAR gamma agonist Pioglitazone improves anatomical and locomotor recovery after rodent spinal cord injury. Exp Neurol 205:3964062007

38

Mu XAzbill RDSpringer JE: Riluzole and methylprednisolone combined treatment improves functional recovery in traumatic spinal cord injury. J Neurotrauma 17:7737802000

39

National Spinal Cord Injury Statistical Center: Spinal Cord Injury Facts and Figures at a Glance Birmingham, ALNSCISC2010. (https://www.nscisc.uab.edu/PublicDocuments/nscisc_home/pdf/Facts%20and%20Figures%20at%20a%20Glance%202010.pdf

40

Nobunaga AIGo BKKarunas RB: Recent demographic and injury trends in people served by the Model Spinal Cord Injury Care Systems. Arch Phys Med Rehabil 80:137213821999

41

Nógrádi ASzabó APintér SVrbová G: Delayed riluzole treatment is able to rescue injured rat spinal motoneurons. Neuroscience 144:4314382007

42

Oberlin CAmeur NETeboul FBeaulieu JYVacher C: Restoration of elbow flexion in brachial plexus injury by transfer of ulnar nerve fascicles to the nerve to the biceps muscle. Tech Hand Up Extrem Surg 6:86902002

43

Ohta SIwashita YTakada HKuno SNakamura T: Neuroprotection and enhanced recovery with edaravone after acute spinal cord injury in rats. Spine (Phila Pa 1976) 30:115411582005

44

Oppenheim JSSpitzer DEWinfree CJ: Spinal cord bypass surgery using peripheral nerve transfers: review of translational studies and a case report on its use following complete spinal cord injury in a human. Experimental article. Neurosurg Focus 26:2E62009

45

Pannu RBarbosa ESingh AKSingh I: Attenuation of acute inflammatory response by atorvastatin after spinal cord injury in rats. J Neurosci Res 79:3403502005

46

Pannu RChristie DKBarbosa ESingh ISingh AK: Posttrauma Lipitor treatment prevents endothelial dysfunction, facilitates neuroprotection, and promotes locomotor recovery following spinal cord injury. J Neurochem 101:1822002007

47

Park SWYi JHMiranpuri GSatriotomo IBowen KResnick DK: Thiazolidinedione class of peroxisome proliferatoractivated receptor gamma agonists prevents neuronal damage, motor dysfunction, myelin loss, neuropathic pain, and inflammation after spinal cord injury in adult rats. J Pharmacol Exp Ther 320:100210122007

48

Pinzon AMarcillo APabon DBramlett HMBunge MBDietrich WD: A re-assessment of erythropoietin as a neuroprotective agent following rat spinal cord compression or contusion injury. Exp Neurol 213:1291362008

49

Ray WZMackinnon SE: Clinical outcomes following median to radial nerve transfers. J Hand Surg Am 36:2012082011

50

Ray WZYarbrough CKYee AMackinnon SE: Clinical outcomes following brachialis to anterior interosseous nerve transfers. J Neurosurg [in press]2012

51

Saganová KOrendácová JCízková DVanický I: Limited minocycline neuroprotection after balloon-compression spinal cord injury in the rat. Neurosci Lett 433:2462492008

52

Sangalang VEBuhr AJMalik HG: Intercostal nerve transfer to lumbar nerve roots. Part II: Neuropathologic findings in the animal model. Spine (Phila Pa 1976) 4:4164221979

53

Schwartz GFehlings MG: Evaluation of the neuroprotective effects of sodium channel blockers after spinal cord injury: improved behavioral and neuroanatomical recovery with riluzole. J Neurosurg 94:2 Suppl2452562001

54

Sönmez AKabakçi BVardar EGürel DSönmez UOrhan YT: Erythropoietin attenuates neuronal injury and potentiates the expression of pCREB in anterior horn after transient spinal cord ischemia in rats. Surg Neurol 68:2973032007

55

Sribnick EASamantaray SDas ASmith JMatzelle DDRay SK: Postinjury estrogen treatment of chronic spinal cord injury improves locomotor function in rats. J Neurosci Res 88:173817502010

56

Stirling DPKhodarahmi KLiu JMcPhail LTMcBride CBSteeves JD: Minocycline treatment reduces delayed oligodendrocyte death, attenuates axonal dieback, and improves functional outcome after spinal cord injury. J Neurosci 24:218221902004

57

Tadie MLiu SRobert RGuiheneuc PPereon YPerrouin-Verbe B: Partial return of motor function in paralyzed legs after surgical bypass of the lesion site by nerve autografts three years after spinal cord injury. J Neurotrauma 19:9099162002

58

Tian DSLiu JLXie MJZhan YQu WSYu ZY: Tamoxifen attenuates inflammatory-mediated damage and improves functional outcome after spinal cord injury in rats. J Neurochem 109:165816672009

59

Tung THMackinnon SE: Nerve transfers: indications, techniques, and outcomes. J Hand Surg Am 35:3323412010

60

Tung THNovak CBMackinnon SE: Nerve transfers to the biceps and brachialis branches to improve elbow flexion strength after brachial plexus injuries. J Neurosurg 98:3133182003

61

Vialle RLacroix CHarding ILoureiro MCTadié M: Motor and sensitive axonal regrowth after multiple intercosto-lumbar neurotizations in a sheep model. Spinal Cord 48:3673742010

62

Vialle RLozeron PLoureiro MCTadié M: Multiple lumbar roots neurotizations with the lower intercostal nerves. Preliminary clinical and electrophysiological results in a sheep model. J Surg Res 149:1992052008

63

Wang XSChen YYShang XFZhu ZGChen GQHan Z: Idazoxan attenuates spinal cord injury by enhanced astrocytic activation and reduced microglial activation in rat experimental autoimmune encephalomyelitis. Brain Res 1253:1982092009

64

Zeman RJBauman WAWen XOuyang NEtlinger JDCardozo CP: Improved functional recovery with oxandrolone after spinal cord injury in rats. Neuroreport 20:8648682009

65

Zhang SJohnston LZhang ZMa YHu YWang J: Restoration of stepping-forward and ambulatory function in patients with paraplegia: rerouting of vascularized intercostal nerves to lumbar nerve roots using selected interfascicular anastomosis. Surg Technol Int 11:2442482003

TrendMD

Metrics

Metrics

All Time Past Year Past 30 Days
Abstract Views 50 50 43
Full Text Views 830 830 426
PDF Downloads 53 53 13
EPUB Downloads 0 0 0

PubMed

Google Scholar