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New Type of Cortical Neuroplasticity After Nerve Repair in Brachial Plexus Lesions

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New Type of Cortical Neuroplasticity After Nerve Repair in Brachial Plexus Lesions OBSERVATION New Type of Cortical Neuroplasticity After Nerve Repair in Brachial Plexus Lesions Roland Beisteiner, MD, MA; Ilse Ho¨llinger, MSc; Jakob Rath, MD; Moritz Wurnig, MSc; Markus Hilbert; Nicolaus Klinger, MSc; Alexander Geißler, MSc, PhD; Florian Fischmeister, PhD; Christian Wo¨ber, MD; Gerhard Klo¨sch, MSc; Hanno Millesi, MD; Wolfgang Grisold, MD; Eduard Auff, MD; Robert Schmidhammer, MD Background: In brachial plexus avulsion, a recent tech- Participants: Three healthy control subjects, 2 pa- nique connects the ending of the disrupted musculocu- tients with phrenic nerve end-to-side coaptation, and 1 taneous nerve to the side of the intact phrenic nerve to control patient with C7 end-to-end coaptation (same clini- regain elbow flexion. This requires the phrenic nerve to cal presentation but phrenic nerve unchanged). perform a new double function: independent control of breathing and elbow flexion. Neuroplastic changes as- Results: Clinical documentation showed that both patients sociated with acquisition of double nerve functions have with phrenic nerve end-to-side coaptation were able to con- not yet been investigated. trolthediaphragmandthebicepsindependentlyviathesame phrenic nerve. In contrast to all controls, both patients with Objective: To evaluate neuroplastic changes associ- phrenic nerve end-to-side coaptation activated the cortical ated with acquisition of double nerve functions in a mono- diaphragm areas with flexion of the diseased arm. functional nerve (phrenic nerve). Conclusion: Our functional magnetic resonance imaging Design: Clinical and functional magnetic resonance data indicate that the patient’s cortical diaphragm areas imaging investigations during arm movements, forced in- reorganize in such a way that independent control of spiration, and motor control tasks. breathing and elbow flexion is possible with the same neu- ronal population. Setting: Investigations at the Medical University of Vienna, Vienna, Austria. Arch Neurol. 2011;68(11):1467-1470 WING TO TOTAL PARESIS nerve targets: muscles originally inner- of the affected arm, vated by the contralateral C7 root or the complete brachial ipsilateral phrenic nerve are denervated. Author Affiliations: Study plexus lesions represent An alternative approach is the nerve fi- Group Clinical fMRI and MR a seriously disabling ber transfer using end-to-side nerve re- 4 Center of Excellence Oneurological condition. In cases of root pair, where the ending of the disrupted (Drs Beisteiner, Rath, Geißler, avulsion, reconstruction of nerve conti- nerve is attached to the side of an intact and Fischmeister, Ms Ho¨llinger, nuity is impossible. To regain at least nerve via an epineurial window. Re- and Messrs Wurnig, Hilbert, partial arm functions, nerve fiber trans- cently, a modified end-to-side procedure and Klinger) and Department of fers that connect axon donors from out- has been suggested where a small motor Neurology (Drs Beisteiner, side the brachial plexus with the affected branch is used to restore motor func- Rath, Geißler, Fischmeister, plexus nerves are increasingly per- tion.5 The major advantage of end-to- Wo¨ber, and Auff, Ms Ho¨llinger, formed. However, the detailed neuro- side nerve repair is preservation of donor and Messrs Wurnig, Hilbert, plastic changes associated with clinical nerve function. In brachial plexus avul- Klinger, and Klo¨sch), Medical 1 University of Vienna, Millesi recovery are yet unknown. There are 2 sion, the ending of the disrupted muscu- Center for Brachial Plexus and major nerve transfer procedures for res- locutaneous nerve can be attached to the Peripheral Nerve Surgery (and toration of elbow flexion in cases of root side of the intact phrenic nerve, thereby Rehabilitation) and Ludwig avulsion. Nerve fibers from the contralat- preserving diaphragm innervation. Such Boltzmann Institute for eral healthy C7 root and nerve fibers patients represent an interesting new Experimental and Clinical from the ipsilateral healthy phrenic model for neuroplasticity: the same Traumatology, Austrian Cluster nerve can be used for reinnervation of phrenic nerve is required to control breath- for Tissue Regeneration the musculocutaneous nerve.2,3 This ing and elbow flexion independently. Al- (Drs Millesi and allows patients to regain elbow flexion of though neuroplastic changes with bra- Schmidhammer), and the paretic arm via contralateral C7 chial plexus injury have already been Department of Neurology and 6,7 Ludwig Boltzmann Institute for inputs or via the ipsilateral phrenic reported, the neuroplastic changes as- Neurooncology, Kaiser Franz nerve. This technique, called end-to-end sociated with acquisition of an additional Josef Hospital (Dr Grisold), nerve repair, has 1 major disadvantage. nerve function are unknown. We hypoth- Vienna, Austria. There is a loss of function in the donor esized that cortical phrenic nerve (dia- ARCH NEUROL / VOL 68 (NO. 11), NOV 2011 WWW.ARCHNEUROL.COM 1467 ©2011 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 Patient 2 was a right-handed man aged 43 years at the time of Control: inspiration a traumatic left complete brachial plexus lesion. He had end-to- side coaptation of (1) the ipsilateral phrenic nerve to (2) the mus- culocutaneous nerve 5 months after trauma. Left elbow flexion was possible against medium resistance at the time of fMRI (7 years after surgery). A general case description including preliminary data analysis is included in the article by Beisteiner et al.8 In both patients with end-to-side nerve repair, the nerve fi- ber transfer from the phrenic nerve to the musculocutaneous nerve was done using 2 sural nerve grafts coapted end to side to the phrenic nerve and end to end to the musculocutaneous Patient 1: inspiration nerve. Every patient provided fully informed consent with a protocol approved by the local ethics committee. HEALTHY CONTROL SUBJECTS To be able to compare fMRI findings of the patients’ reorga- nized nervous systems with unchanged nervous systems, fMRI recordings were also performed in 3 male healthy control sub- jects aged 42, 27, and 22 years without any history of nervous system disease. Patient 2: inspiration Expiration CLINICAL DOCUMENTATION In the control patient with C7 end-to-end coaptation, chest ra- diography documented a normal bilateral diaphragm innerva- tion with deep inspiration (Figure 1). Electromyography of the affected biceps muscle demonstrated independence of muscle innervation and breathing (Figure 2B). In patient 1 with phrenic nerve end-to-side coaptation, video recording showed a lack of biceps contractions with deep in- spiration or coughing and no change of breathing patterns with elbow flexion. Chest radiography documented bilateral dia- Figure 1. Chest radiographs of participants (the left side of the images are phragm innervation with deep inspiration and no elevated dia- the right side of the participants). The control patient with C7 end-to-end phragm (Figure 1). Electromyography of the affected biceps coaptation shows normal bilateral diaphragm innervation with inspiration. Patient 1 with phrenic nerve end-to-side coaptation shows preserved bilateral muscle demonstrated independence of muscle innervation and diaphragm innervation. Patient 2 with phrenic nerve end-to-side coaptation breathing. shows preserved innervation but diaphragm elevation on the operated left In patient 2 with phrenic nerve end-to-side coaptation, video side. With inspiration, contraction of the left diaphragm produces a shift of recording and fluoroscopy of the thorax showed a lack of bi- about 2 intercostal spaces. ceps contractions with deep inspiration or coughing and a lack of diaphragm innervation with elbow flexion. Chest radiogra- phragm) representations reorganize in such a pattern that phy documented an elevated but innervated diaphragm on the independent control of breathing and elbow flexion is affected side (Figure 1). Electromyography of the affected bi- possible with the same neuronal population.8 Herein, we ceps muscle demonstrated independence of muscle innerva- present comprehensive functional magnetic resonance tion and breathing (Figure 2A). During forced inspiration and imaging (fMRI) studies of 2 patients with phrenic nerve coughing, spikes of motor activation appeared in very few parts end-to-side coaptation, 1 control patient with C7 end- of the electromyographic recordings. to-end coaptation, and 3 healthy control subjects to test this hypothesis. FUNCTIONAL MRI Investigations included 4 tasks: (1) elbow flexion of the dis- METHODS eased arm; (2) elbow flexion of the healthy arm; (3) forced ab- dominal inspiration; and (4) foot flexion on the side of the dis- PATIENTS eased arm. Patient 1 with phrenic nerve end-to-side coaptation per- The control patient was a right-handed boy aged 6 years at the formed tasks 1 through 4, patient 2 with phrenic nerve end- time of a traumatic left complete brachial plexus lesion. He had to-side coaptation and the healthy control subjects performed end-to-end coaptation of (1) contralateral root C7 to (2) the tasks 1 and 2, and the control patient with C7 end-to-end co- musculocutaneous nerve 5 months after trauma. Left elbow flex- aptation performed tasks 1 through 3. Repetitive investiga- ion was possible against light resistance at the time of fMRI (6.5 tions were performed with 3-T MRI and 7-T MRI (blood oxy- years after surgery). gen level–dependent gradient echo–echo planar imaging; 34 Patient 1 was a right-handed woman aged 29 years
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