Moore, Amy M

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Nerve Transfers to Restore Upper Extremity Function: A Paradigm Shift

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Washington University School of MedicineDigital Commons@BeckerOpen Access Publications2014Nerve transfers to restore upper extremity function:A paradigm shiftAmy M. MooreWashington University School of Medicine in St. LouisFollow this and additional works at: http://digitalcommons.wustl.edu/open_access_pubsThis Open Access Publication is brought to you for free and open access by Digital Commons@Becker. It has been accepted for inclusion in OpenAccess Publications by an authorized administrator of Digital Commons@Becker. For more information, please contact engeszer@wustl.edu.Recommended CitationMoore, Amy M., ,"Nerve transfers to restore upper extremity function: A paradigm shift." Frontiers in Neurology.5,. 40. (2014).http://digitalcommons.wustl.edu/open_access_pubs/2770                                                         OPINION ARTICLEpublished: 31 March 2014doi: 10.3389/fneur.2014.00040Nerve transfers to restore upper extremity function:a paradigm shiftAmy M. Moore*Plastic and Reconstructive Surgery,Washington University School of Medicine, St. Louis, MO, USA*Correspondence: mooream@wustl.eduEdited and reviewed by:Renée Morris, University of New SouthWales, AustraliaKeywords: nerve transfer, brachial plexus injury, peripheral nerve injury, surgical procedures, operative, upper extremity, hand function, upper extremityfunctionBrachial plexus and peripheral nerveinjuries lead to significant upper extremitydysfunction and disability. Traditionally,both have been treated with nerve graft-ing when a tensionless, end-to-end repairis not feasible. Despite our best efforts,functional outcomes of this procedure areless than ideal due to the long distancesthat the axons must regenerate to reachtheir end organs. Over the past 20 years ourunderstanding of nerve anatomy, topogra-phy, and regeneration has improved andthe surgical technique of nerve transfershas been developed. Due to improved func-tional outcomes, decreased morbidity, andsurgical time, we are now experiencing aparadigm shift in the treatment of brachialplexus and peripheral nerve injuries fromnerve grafting to nerve transfers (1, 2).Motor function after nerve injury isdependent on both time to reinnervationand the number of motor axons reinner-vating the target muscle (3). Nerve trans-fers capitalize on these two factors and arethe reason for their clinical success. Nervetransfers, by definition, involve coapting ahealthy, expendable donor nerve or fascicleto a denervated recipient nerve to restorefunction to the recipient end-organ (skinfor sensation or muscle for motor func-tion). They can be performed closer to therecipient target allowing for earlier reinner-vation of the muscle and quicker return offunction. Further advantages include thatnerve transfers are performed outside thezone of injury and scarred field, can be per-formed on patients with delayed presenta-tion, and can avoid interpositional nervegrafting, which leads to increased numbersof regenerating nerve fibers making it tothe target organ (3).The ideal timing of nerve transfers hasnot yet been established, but reinnervationof the muscle by 12–18 months after injuryis a common goal. Indications are evolv-ing and currently include patients withproximal nerve root avulsions, high levelperipheral nerve injuries, large neuromas-in-continuity, and/or multi-level nerveinjuries. In our group, we use nerve trans-fers to treat most brachial plexus injuries(avulsions or not) and peripheral nerveinjuries in upper arm or proximal fore-arm. We usually reserve nerve grafting fornerve injuries in the distal forearm or handbecause the regenerative distances and timeto reinnervation of the muscle are short. Atthese distal injuries, functional outcomeswith grafting are similar to those seen withnerve transfers and donor site morbidityfrom a nerve transfer is avoided.In brachial plexus injuries, a hierar-chy of return of function exists withefforts directed to restoring elbow flexionfirst, followed by shoulder function, thenhand function. For upper trunk injuries,multiple combinations of nerve transfershave been described. The double fascicularnerve transfer is the most common nervetransfer performed to return elbow flexion.This transfer involves coapting redundantnerve fascicles from the median and ulnarnerves to the biceps brachii and brachialisbranches of the musculocutaneous nerve.Many have reported their experience withthis transfer and patients have achievedat least Medical Research Council (MRC)strength of 3 with most achieving grade4 or greater without evidence of donorsite morbidity (4–6). For restoration ofshoulder function transfers of the spinalaccessory nerve to the suprascapular nerveand a branch of the triceps to the axil-lary nerve are most commonly performed.Thoracodorsal nerve and intercostal nervestransferred to the long thoracic nerve arealso common to restore scapular stabil-ity provided by the serratus anterior mus-cle. Restoration of shoulder abductionand external rotation has been successfullyreported with these nerve transfers (7, 8).In lower plexus injuries, the brachialisbranch of the musculocutaneous nerve canbe transferred with encouraging results tothe anterior interosseous nerve to restoreprehension. Previously, these lower plexusinjuries were treated with free functionalmuscle transfers given the great regen-erative distance from the brachial plexusto the forearm musculature. However,free functional muscle transfers are asso-ciated with increased morbidity, opera-tive time, and lengthy hospital stays. Thebrachialis to anterior interosseous nervetransfer avoids these drawbacks and estab-lishes a platform for restoring functionto the hand.In addition to their use for brachialplexus injuries, nerve transfers to restorehand function following peripheral nerveinjuries are also gaining momentum. Newtransfers continue to be developed as ourunderstanding of nerve topography grows.Ulnar nerve injuries result in loss of powergrip, pinch strength, and hand dexterity.The pronator quadratus branch of theanterior interosseous nerve can be trans-ferred to the motor component of the ulnarnerve distally in the forearm to reinner-vate the intrinsic muscles of the hand (9).It was originally described as an end-to-end coaptation if no regeneration of theulnar nerve is expected, but recently Mack-innon and colleagues have shown effi-cacy of an end-to-side “supercharge” coap-tation enabling proximal regeneration ofthe ulnar nerve to proceed as well (10).Upper extremity trauma frequently resultsin radial nerve injuries impairing bothwww.frontiersin.org March 2014 | Volume 5 | Article 40 | 1                                                         Moore Nerve transfers restore functionwrist and finger extension. Although ten-don transfers are functional for patientswith radial nerve palsies, nerve transfersfrom the median to radial nerves allowfor independent thumb and finger exten-sion (11). To restore median nerve func-tion, transfer of branches of the radialnerve, the brachialis branch, and branchesof the ulnar nerve have been described withgood outcomes (12). Focusing on syner-gism and redundancy of function has ledto the success of these transfers.An exciting application of nerve trans-fers is in the field of spinal cord injury(SCI). Drs. Susan Mackinnon and Ida Foxat Washington University in St. Louis, MO,USA are leading developers in the use ofnerve transfers to restore upper extrem-ity function in patients with cervical SCI.These transfers are being developed toincrease volitional control and improveindependence. Unlike brachial plexus orperipheral nerve injuries, SCI patients haveintact lower motoneurons below the levelof injury and thus, the motoneuron –peripheral nerve – muscle end-organ con-nection remains intact. For this reason,the muscle is “preserved” and nerve trans-fers in SCI patients can be performedwithout the time sensitivity found with aperipheral nerve injury. Specific transfersfor SCI include transfer of the brachialisbranch of the musculocutaneous nerve tothe anterior interosseous nerve to improveprehension and transfer of the deltoidnerve branches to the triceps branches toimprove elbow extension. Evaluation andcollaboration among the physiatrists, ther-apists, and surgeon are critical to identi-fying ideal candidates, developing opera-tive plans, and ultimately achieving suc-cess with nerve transfers in this patientpopulation.In conclusion, nerve transfers are anessential tool for the peripheral nerve sur-geon to improve upper extremity func-tion after nerve injury. I would argue thatnerve transfers are the preferred treatmentfor high peripheral nerve injuries and formost patterns of brachial plexus injury. Inaddition, they will likely play an increas-ing role in managing SCI patients. Returnof earlier, more effective upper extremityfunction supports the importance of thissurgical technique. As we critically analyzeand report our outcomes with nerve trans-fers, further indications and expectationsof return of function will be elucidated.The paradigm shift; however, is happeningnow. Nerve transfers viewed as“standard ofcare” may not be far away. Currently, theycertainly hold great promise and shouldbe considered in restoring upper extremityfunction in patients with devastating nerveinjuries.REFERENCES1. Garg R, Merrell GA, Hillstrom HJ, Wolfe SW.Comparison of nerve transfers and nerve graft-ing for traumatic upper plexus palsy: a systematicreview and analysis. J Bone Joint Surg Am (2011)93:819–29. doi:10.2106/JBJS.I.016022. Yang LJ, Chang KW, Chung KC. A systematicreview of nerve transfer and nerve repair for thetreatment of adult upper brachial plexus injury.Neurosurgery (2012) 71:417–29. doi:10.1227/NEU.0b013e318257be98 discussion 429,3. Tung TH, Mackinnon SE. Nerve transfers: indica-tions, techniques, and outcomes. J Hand Surg Am(2010) 35:332–41. doi:10.1016/j.jhsa.2009.12.0024. Belzberg AJ, Dorsi MJ, Storm PB, Moriarity JL.Surgical repair of brachial plexus injury: a multi-national survey of experienced peripheral nervesurgeons. J Neurosurg (2004) 101:365–76. doi:10.3171/jns.2004.101.3.03655. Teboul F, Kakkar R, Ameur N, Beaulieu JY, Ober-lin C. Transfer of fascicles from the ulnar nerve tothe nerve to the biceps in the treatment of upperbrachial plexus palsy. J Bone Joint Surg Am (2004)86-A:1485–90.6. Ray WZ,Pet MA,Yee A,Mackinnon SE. Double fas-cicular nerve transfer to the biceps and brachialismuscles after brachial plexus injury: clinical out-comes in a series of 29 cases. J Neurosurg (2011)114:1520–8. doi:10.3171/2011.1.JNS108107. Leechavengvongs S, Witoonchart K, UerpairojkitC, Thuvasethakul P. Nerve transfer to deltoid mus-cle using the nerve to the long head of the tri-ceps, part II: a report of 7 cases. J Hand SurgAm (2003) 28:633–8. doi:10.1016/S0363-5023(03)00199-08. Bertelli JA, Ghizoni MF. Reconstruction of C5 andC6 brachial plexus avulsion injury by multiplenerve transfers: spinal accessory to suprascapular,ulnar fascicles to biceps branch, and triceps longor lateral head branch to axillary nerve. J HandSurg Am (2004) 29:131–9. doi:10.1016/j.jhsa.2003.10.0139. Wang Y, Zhu S. Transfer of a branch of the ante-rior interosseus nerve to the motor branch of themedian nerve and ulnar nerve. Chin Med J (Engl)(1997) 110:216–9.10. Barbour J, Yee A, Kahn LC, Mackinnon SE. Super-charged end-to-side anterior interosseous to ulnarmotor nerve transfer for intrinsic musculaturereinnervation. J Hand Surg Am (2012) 37:2150–9.doi:10.1016/j.jhsa.2012.07.02211. Ray WZ, Mackinnon SE. Clinical outcomes fol-lowing median to radial nerve transfers. J HandSurg Am (2011) 36:201–8. doi:10.1016/j.jhsa.2010.09.03412. Brown JM, Mackinnon SE. Nerve transfers in theforearm and hand. Hand Clin (2008) 24:319–40.doi:10.1016/j.hcl.2008.08.002Received: 27 February 2014; accepted: 18 March 2014;published online: 31 March 2014.Citation: Moore AM (2014) Nerve transfers to restoreupper extremity function: a paradigm shift. Front.Neurol. 5:40. doi: 10.3389/fneur.2014.00040This article was submitted to Movement Disorders, asection of the journal Frontiers in Neurology.Copyright © 2014 Moore. This is an open-access articledistributed under the terms of the Creative CommonsAttribution License (CC BY). The use, distribution orreproduction in other forums is permitted, provided theoriginal author(s) or licensor are credited and that theoriginal publication in this journal is cited, in accordancewith accepted academic practice. No use, distribution orreproduction is permitted which does not comply withthese terms.Frontiers in Neurology | Movement Disorders March 2014 | Volume 5 | Article 40 | 2

Nerve transfers to restore upper extremity function: A paradigm shift

Frontiers - Publisher Connector

  
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
OPINION ARTICLE
published: 31 March 2014
doi: 10.3389/fneur.2014.00040
Nerve transfers to restore upper extremity function:
a paradigm shift
Amy M. Moore*
Plastic and Reconstructive Surgery,Washington University School of Medicine, St. Louis, MO, USA
*Correspondence: mooream@wustl.edu
Edited and reviewed by:
Renée Morris, University of New SouthWales, Australia
Keywords: nerve transfer, brachial plexus injury, peripheral nerve injury, surgical procedures, operative, upper extremity, hand function, upper extremity
function
Brachial plexus and peripheral nerve
injuries lead to significant upper extremity
dysfunction and disability. Traditionally,
both have been treated with nerve graft-
ing when a tensionless, end-to-end repair
is not feasible. Despite our best efforts,
functional outcomes of this procedure are
less than ideal due to the long distances
that the axons must regenerate to reach
their end organs. Over the past 20 years our
understanding of nerve anatomy, topogra-
phy, and regeneration has improved and
the surgical technique of nerve transfers
has been developed. Due to improved func-
tional outcomes, decreased morbidity, and
surgical time, we are now experiencing a
paradigm shift in the treatment of brachial
plexus and peripheral nerve injuries from
nerve grafting to nerve transfers (1, 2).
Motor function after nerve injury is
dependent on both time to reinnervation
and the number of motor axons reinner-
vating the target muscle (3). Nerve trans-
fers capitalize on these two factors and are
the reason for their clinical success. Nerve
transfers, by definition, involve coapting a
healthy, expendable donor nerve or fascicle
to a denervated recipient nerve to restore
function to the recipient end-organ (skin
for sensation or muscle for motor func-
tion). They can be performed closer to the
recipient target allowing for earlier reinner-
vation of the muscle and quicker return of
function. Further advantages include that
nerve transfers are performed outside the
zone of injury and scarred field, can be per-
formed on patients with delayed presenta-
tion, and can avoid interpositional nerve
grafting, which leads to increased numbers
of regenerating nerve fibers making it to
the target organ (3).
The ideal timing of nerve transfers has
not yet been established, but reinnervation
of the muscle by 12–18 months after injury
is a common goal. Indications are evolv-
ing and currently include patients with
proximal nerve root avulsions, high level
peripheral nerve injuries, large neuromas-
in-continuity, and/or multi-level nerve
injuries. In our group, we use nerve trans-
fers to treat most brachial plexus injuries
(avulsions or not) and peripheral nerve
injuries in upper arm or proximal fore-
arm. We usually reserve nerve grafting for
nerve injuries in the distal forearm or hand
because the regenerative distances and time
to reinnervation of the muscle are short. At
these distal injuries, functional outcomes
with grafting are similar to those seen with
nerve transfers and donor site morbidity
from a nerve transfer is avoided.
In brachial plexus injuries, a hierar-
chy of return of function exists with
efforts directed to restoring elbow flexion
first, followed by shoulder function, then
hand function. For upper trunk injuries,
multiple combinations of nerve transfers
have been described. The double fascicular
nerve transfer is the most common nerve
transfer performed to return elbow flexion.
This transfer involves coapting redundant
nerve fascicles from the median and ulnar
nerves to the biceps brachii and brachialis
branches of the musculocutaneous nerve.
Many have reported their experience with
this transfer and patients have achieved
at least Medical Research Council (MRC)
strength of 3 with most achieving grade
4 or greater without evidence of donor
site morbidity (4–6). For restoration of
shoulder function transfers of the spinal
accessory nerve to the suprascapular nerve
and a branch of the triceps to the axil-
lary nerve are most commonly performed.
Thoracodorsal nerve and intercostal nerves
transferred to the long thoracic nerve are
also common to restore scapular stabil-
ity provided by the serratus anterior mus-
cle. Restoration of shoulder abduction
and external rotation has been successfully
reported with these nerve transfers (7, 8).
In lower plexus injuries, the brachialis
branch of the musculocutaneous nerve can
be transferred with encouraging results to
the anterior interosseous nerve to restore
prehension. Previously, these lower plexus
injuries were treated with free functional
muscle transfers given the great regen-
erative distance from the brachial plexus
to the forearm musculature. However,
free functional muscle transfers are asso-
ciated with increased morbidity, opera-
tive time, and lengthy hospital stays. The
brachialis to anterior interosseous nerve
transfer avoids these drawbacks and estab-
lishes a platform for restoring function
to the hand.
In addition to their use for brachial
plexus injuries, nerve transfers to restore
hand function following peripheral nerve
injuries are also gaining momentum. New
transfers continue to be developed as our
understanding of nerve topography grows.
Ulnar nerve injuries result in loss of power
grip, pinch strength, and hand dexterity.
The pronator quadratus branch of the
anterior interosseous nerve can be trans-
ferred to the motor component of the ulnar
nerve distally in the forearm to reinner-
vate the intrinsic muscles of the hand (9).
It was originally described as an end-to-
end coaptation if no regeneration of the
ulnar nerve is expected, but recently Mack-
innon and colleagues have shown effi-
cacy of an end-to-side “supercharge” coap-
tation enabling proximal regeneration of
the ulnar nerve to proceed as well (10).
Upper extremity trauma frequently results
in radial nerve injuries impairing both
www.frontiersin.org March 2014 | Volume 5 | Article 40 | 1
  
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
Moore Nerve transfers restore function
wrist and finger extension. Although ten-
don transfers are functional for patients
with radial nerve palsies, nerve transfers
from the median to radial nerves allow
for independent thumb and finger exten-
sion (11). To restore median nerve func-
tion, transfer of branches of the radial
nerve, the brachialis branch, and branches
of the ulnar nerve have been described with
good outcomes (12). Focusing on syner-
gism and redundancy of function has led
to the success of these transfers.
An exciting application of nerve trans-
fers is in the field of spinal cord injury
(SCI). Drs. Susan Mackinnon and Ida Fox
at Washington University in St. Louis, MO,
USA are leading developers in the use of
nerve transfers to restore upper extrem-
ity function in patients with cervical SCI.
These transfers are being developed to
increase volitional control and improve
independence. Unlike brachial plexus or
peripheral nerve injuries, SCI patients have
intact lower motoneurons below the level
of injury and thus, the motoneuron –
peripheral nerve – muscle end-organ con-
nection remains intact. For this reason,
the muscle is “preserved” and nerve trans-
fers in SCI patients can be performed
without the time sensitivity found with a
peripheral nerve injury. Specific transfers
for SCI include transfer of the brachialis
branch of the musculocutaneous nerve to
the anterior interosseous nerve to improve
prehension and transfer of the deltoid
nerve branches to the triceps branches to
improve elbow extension. Evaluation and
collaboration among the physiatrists, ther-
apists, and surgeon are critical to identi-
fying ideal candidates, developing opera-
tive plans, and ultimately achieving suc-
cess with nerve transfers in this patient
population.
In conclusion, nerve transfers are an
essential tool for the peripheral nerve sur-
geon to improve upper extremity func-
tion after nerve injury. I would argue that
nerve transfers are the preferred treatment
for high peripheral nerve injuries and for
most patterns of brachial plexus injury. In
addition, they will likely play an increas-
ing role in managing SCI patients. Return
of earlier, more effective upper extremity
function supports the importance of this
surgical technique. As we critically analyze
and report our outcomes with nerve trans-
fers, further indications and expectations
of return of function will be elucidated.
The paradigm shift; however, is happening
now. Nerve transfers viewed as“standard of
care” may not be far away. Currently, they
certainly hold great promise and should
be considered in restoring upper extremity
function in patients with devastating nerve
injuries.
REFERENCES
1. Garg R, Merrell GA, Hillstrom HJ, Wolfe SW.
Comparison of nerve transfers and nerve graft-
ing for traumatic upper plexus palsy: a systematic
review and analysis. J Bone Joint Surg Am (2011)
93:819–29. doi:10.2106/JBJS.I.01602
2. Yang LJ, Chang KW, Chung KC. A systematic
review of nerve transfer and nerve repair for the
treatment of adult upper brachial plexus injury.
Neurosurgery (2012) 71:417–29. doi:10.1227/NEU.
0b013e318257be98 discussion 429,
3. Tung TH, Mackinnon SE. Nerve transfers: indica-
tions, techniques, and outcomes. J Hand Surg Am
(2010) 35:332–41. doi:10.1016/j.jhsa.2009.12.002
4. Belzberg AJ, Dorsi MJ, Storm PB, Moriarity JL.
Surgical repair of brachial plexus injury: a multi-
national survey of experienced peripheral nerve
surgeons. J Neurosurg (2004) 101:365–76. doi:10.
3171/jns.2004.101.3.0365
5. Teboul F, Kakkar R, Ameur N, Beaulieu JY, Ober-
lin C. Transfer of fascicles from the ulnar nerve to
the nerve to the biceps in the treatment of upper
brachial plexus palsy. J Bone Joint Surg Am (2004)
86-A:1485–90.
6. Ray WZ,Pet MA,Yee A,Mackinnon SE. Double fas-
cicular nerve transfer to the biceps and brachialis
muscles after brachial plexus injury: clinical out-
comes in a series of 29 cases. J Neurosurg (2011)
114:1520–8. doi:10.3171/2011.1.JNS10810
7. Leechavengvongs S, Witoonchart K, Uerpairojkit
C, Thuvasethakul P. Nerve transfer to deltoid mus-
cle using the nerve to the long head of the tri-
ceps, part II: a report of 7 cases. J Hand Surg
Am (2003) 28:633–8. doi:10.1016/S0363-5023(03)
00199-0
8. Bertelli JA, Ghizoni MF. Reconstruction of C5 and
C6 brachial plexus avulsion injury by multiple
nerve transfers: spinal accessory to suprascapular,
ulnar fascicles to biceps branch, and triceps long
or lateral head branch to axillary nerve. J Hand
Surg Am (2004) 29:131–9. doi:10.1016/j.jhsa.2003.
10.013
9. Wang Y, Zhu S. Transfer of a branch of the ante-
rior interosseus nerve to the motor branch of the
median nerve and ulnar nerve. Chin Med J (Engl)
(1997) 110:216–9.
10. Barbour J, Yee A, Kahn LC, Mackinnon SE. Super-
charged end-to-side anterior interosseous to ulnar
motor nerve transfer for intrinsic musculature
reinnervation. J Hand Surg Am (2012) 37:2150–9.
doi:10.1016/j.jhsa.2012.07.022
11. Ray WZ, Mackinnon SE. Clinical outcomes fol-
lowing median to radial nerve transfers. J Hand
Surg Am (2011) 36:201–8. doi:10.1016/j.jhsa.2010.
09.034
12. Brown JM, Mackinnon SE. Nerve transfers in the
forearm and hand. Hand Clin (2008) 24:319–40.
doi:10.1016/j.hcl.2008.08.002
Received: 27 February 2014; accepted: 18 March 2014;
published online: 31 March 2014.
Citation: Moore AM (2014) Nerve transfers to restore
upper extremity function: a paradigm shift. Front.
Neurol. 5:40. doi: 10.3389/fneur.2014.00040
This article was submitted to Movement Disorders, a
section of the journal Frontiers in Neurology.
Copyright © 2014 Moore. This is an open-access article
distributed under the terms of the Creative Commons
Attribution License (CC BY). The use, distribution or
reproduction in other forums is permitted, provided the
original author(s) or licensor are credited and that the
original publication in this journal is cited, in accordance
with accepted academic practice. No use, distribution or
reproduction is permitted which does not comply with
these terms.
Frontiers in Neurology | Movement Disorders March 2014 | Volume 5 | Article 40 | 2


Nerve Transfers to Restore upper Extremity Function: A Paradigm Shift

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Nerve transfers to restore upper extremity function: A paradigm shift

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