Review of outcomes measures used to evaluate upper extremity surgical treatment of cervical spinal cord injury with recommendations for the future

Abstract

Cervical spinal cord injury is a life-altering event that profoundly affects an individual’s upper extremity function. Nerve transfer surgeries have been shown to restore more natural movement and fine motor control in this population. At present, there is no consensus on how to evaluate the efficacy of these restorative surgeries. The purpose of this work was to perform a comprehensive review of the existing literature and describe the outcome measures used. We hypothesized that the assessments will be heterogeneous across studies and will incompletely capture the effect of nerve transfers on upper extremity motion in cervical spinal cord injury. A search strategy was designed and a review of multiple databases (Embase.com, Ovid-Medline All, and Scopus) yielded 481 articles; 26 unique studies met inclusion criteria and underwent analysis. Both manual muscle strength testing and video content were presented in the majority of studies. Outcome assessments including myometry, functional outcomes measures (such as the grasp and release test), patient-reported outcomes (including generic, extremity, and disease-specific types), and custom de novo questionnaires were used variably across studies. Future work should focus on standardizing outcomes measures in the field and developing and incorporating kinematic analysis to quantify the intricate, coordinated, and precise movement attained after nerve transfer surgery in the setting of cervical spinal cord injury.

Keywords

Nerve transfer surgery / upper extremity function / cervical spinal cord injury / tetraplegia / outcome assessments / kinematic analysis

References

[1] Ackery A,Krassioukov A.A global perspective on spinal cord injury epidemiology.J Neurotrauma2004;21:1355-70

[2] Jain NB,Peterson EN.Traumatic spinal cord injury in the United States, 1993-2012.JAMA2015;313:2236-43 PMCID:PMC4712685

[3] National Spinal Cord Injury Statistical Center. Traumatic spinal cord injury facts and figures at a glance. Available from: https://msktc.org/sites/default/files/SCI-Facts-Figs-2022-Eng-508.pdf [Last accessed on 20 Feb 2024]

[4] Kramer JL,Schubert M,Steeves JD.Relationship between motor recovery and independence after sensorimotor-complete cervical spinal cord injury.Neurorehabil Neural Repair2012;26:1064-71

[5] Dengler J,Steeves JD.Department of Defense (DOD) GroupEuropean Multicenter Study of Spinal Cord Injury (EMSCI) GroupEvaluation of functional independence in cervical spinal cord injury: implications for surgery to restore upper limb function.J Hand Surg Am2021;46:621.e1-17

[6] Dengler J,Curt A,Novak CB.DOD consortiumEMSCI consortiumSpontaneous motor recovery after cervical spinal cord injury: issues for nerve transfer surgery decision making.Spinal Cord2022;60:922-7

[7] Drew L.Abandoned: the human cost of neurotechnology failure.Nature2022;Online ahead of print.

[8] Zlotolow DA.The role of the upper extremity surgeon in the management of tetraplegia.J Hand Surg Am2011;36:929-35; quiz 935

[9] Kozin SH.Biceps-to-triceps transfer for restoration of elbow extension in tetraplegia.Tech Hand Up Extrem Surg2003;7:43-51

[10] Hawasli AH,Reynolds MR.Transfer of the brachialis to the anterior interosseous nerve as a treatment strategy for cervical spinal cord injury: technical note.Global Spine J2015;5:110-7 PMCID:PMC4369208

[11] Fox IK,Novak CB.Nerve transfers to restore upper extremity function in cervical spinal cord injury: update and preliminary outcomes.Plast Reconstr Surg2015;136:780-92

[12] Fox IK,Novak CB.Use of peripheral nerve transfers in tetraplegia: evaluation of feasibility and morbidity.Hand2015;10:60-7 PMCID:PMC4349853

[13] Fridén J.Brachialis-to-extensor carpi radialis longus selective nerve transfer to restore wrist extension in tetraplegia: case report.J Hand Surg Am2012;37:1606-8

[14] Mackinnon SE,Ray WZ.Nerve transfers for the restoration of hand function after spinal cord injury.J Neurosurg2012;117:176-85

[15] van Zyl N,Cooper CA,Flood SJ.Upper limb reinnervation in C6 tetraplegia using a triple nerve transfer: case report.J Hand Surg Am2014;39:1779-83

[16] Khalifeh JM,Van Voorhis A.Nerve transfers in the upper extremity following cervical spinal cord injury. Part 1: Systematic review of the literature.J Neurosurg Spine2019;:1-12

[17] Bertelli JA.Nerve transfers for elbow and finger extension reconstruction in midcervical spinal cord injuries.J Neurosurg2015;122:121-7

[18] Bertelli JA.Nerve transfers for restoration of finger flexion in patients with tetraplegia.J Neurosurg Spine2017;26:55-61

[19] Leclercq C.[Surgical rehabilitation of the upper limbs in tetraplegic patients].Chirurgie1996;121:492-5

[20] Benassy J.A case of transposition of the musculo-cutaneous nerve upon the median nerve.Paraplegia1965;3:199-202

[21] Kiwerski J.Recovery of simple hand function in tetraplegia patients following transfer of the musculo-cutaneous nerve into the median nerve.Paraplegia1982;20:242-7

[22] Mulcahey MJ,Kozin S.Assessment of upper limb in tetraplegia: considerations in evaluation and outcomes research.J Rehabil Res Dev2007;44:91-102

[23] van Zyl N,Cooper C,Galea MP.Expanding traditional tendon-based techniques with nerve transfers for the restoration of upper limb function in tetraplegia: a prospective case series.Lancet2019;394:565-75

[24] Alderman AK.Measuring outcomes in hand surgery.Clin Plast Surg2008;35:239-50 PMCID:PMC3544475

[25] Moberg E,House JH.Third international conference on surgical rehabilitation of the upper limb in tetraplegia (quadriplegia).J Hand Surg Am1989;14:1064-6

[26] Bertelli JA,Winkelmann Duarte EC,Duarte H.Transfer of axillary nerve branches to reconstruct elbow extension in tetraplegics: a laboratory investigation of surgical feasibility.Microsurgery2011;31:376-81

[27] Bertelli JA,Ghizoni MF,Santos MA.Transfer of supinator motor branches to the posterior interosseous nerve to reconstruct thumb and finger extension in tetraplegia: case report.J Hand Surg Am2010;35:1647-51

[28] Bertelli JA,Tacca CP,Ghizoni MF.Transfer of the distal terminal motor branch of the extensor carpi radialis brevis to the nerve of the flexor pollicis longus: an anatomic study and clinical application in a tetraplegic patient.Neurosurgery2012;70:1011-6; discussion 1016

[29] Bertelli JA.Single-stage surgery combining nerve and tendon transfers for bilateral upper limb reconstruction in a tetraplegic patient: case report.J Hand Surg Am2013;38:1366-9

[30] Hawasli AH,Reynolds MR.Transfer of the brachialis to the anterior interosseous nerve as a treatment strategy for cervical spinal cord injury: technical note.Global Spine J2015;5:110-7. PMCID:PMC4369208

[31] Bertelli JA.Nerve and free gracilis muscle transfers for thumb and finger extension reconstruction in long-standing tetraplegia.J Hand Surg Am2016;41:e411-6

[32] Emamhadi M.Double nerve transfer for restoration of hand grasp and release in C7 tetraplegia following complete cervical spinal cord injury.Acta Neurochir2018;160:2219-24

[33] Fox IK,Kahn LC,Ruvinskaya R.Using nerve transfer to restore prehension and grasp 12 years following spinal cord injury: a case report.Spinal Cord Ser Cases2018;4:37 PMCID:PMC5920054

[34] Dibble CF,VanVoorhis A,Ray WZ.Novel nerve transfers for motor and sensory restoration in high cervical spinal cord injury.World Neurosurg2019;128:611-615.e1

[35] Biondi M,Bigazzi P,Pfanner S.Combined nerve and tendon transfer to restore elbow extension in tetraplegic patients: surgical technique and case report.Spinal Cord Ser Cases2020;6:31 PMCID:PMC7193586

[36] van Zyl N,Cooper C,Hill B.Transfer of the supinator nerve to the posterior interosseous nerve for hand opening in tetraplegia through an anterior approach.J Hand Surg Eur Vol2021;46:717-24

[37] Waris E,Palmgren-Soppela T.Transfer of the supinator nerve to the extensor carpi radialis brevis nerve for wrist extension in high tetraplegia.J Hand Surg Eur Vol2021;46:894-6

[38] Paternostro-Sluga T,Posch M.Reliability and validity of the medical research council (MRC) scale and a modified scale for testing muscle strength in patients with radial palsy.J Rehabil Med2008;40:665-71

[39] Aids to the Examination of the Peripheral Nervous System. Available from: https://www.ukri.org/wp-content/uploads/2021/12/MRC-011221-AidsToTheExaminationOfThePeripheralNervousSystem.pdf [Last accessed on 20 Feb 2024]

[40] Polkey CE.Book Reviews.British Medical Bulletin1977;33:182

[41] Stark T,Phillips JK,Beck R.Hand-held dynamometry correlation with the gold standard isokinetic dynamometry: a systematic review.PM R2011;3:472-9

[42] Herbison GJ,Cohen ME.Strength post-spinal cord injury: myometer vs manual muscle test.Spinal Cord1996;34:543-8

[43] Waris E,Sommarhem A.Nerve transfer of brachialis branch to anterior interosseus nerve using in situ lateral antebrachial cutaneous nerve graft in tetraplegia.J Hand Surg Am2022;47:390.e1-7

[44] Sollerman C.Sollerman hand function test. A standardised method and its use in tetraplegic patients.Scand J Plast Reconstr Surg Hand Surg1995;29:167-76

[45] Kalsi-Ryan S,Curt A.The graded redefined assessment of strength sensibility and prehension: reliability and validity.J Neurotrauma2012;29:905-14

[46] Wuolle KS,Thrope GB,Peckham PH.Development of a quantitative hand grasp and release test for patients with tetraplegia using a hand neuroprosthesis.J Hand Surg Am1994;19:209-18

[47] Javeed S,Greenberg JK.Upper limb nerve transfer surgery in patients with tetraplegia.JAMA Netw Open2022;5:e2243890 PMCID:PMC9706368

[48] Lyle RC.A performance test for assessment of upper limb function in physical rehabilitation treatment and research.Int J Rehabil Res1981;4:483-92

[49] Velstra IM,Tanadini LG.Prediction and stratification of upper limb function and self-care in acute cervical spinal cord injury with the graded redefined assessment of strength, sensibility, and prehension (GRASSP).Neurorehabil Neural Repair2014;28:632-42

[50] Sacco C,Visani J.Functional outcome after transfer of brachialis on anterior interosseous and supinator on posterior interosseous nerves: a preliminary report.Microsurgery2022;42:577-85

[51] Mulcahey MJ,Betz RR.Psychometric rigor of the grasp and release test for measuring functional limitation of persons with tetraplegia: a preliminary analysis.J Spinal Cord Med2004;27:41-6.

[52] Fitzpatrick R,Buxton MJ.Evaluating patient-based outcome measures for use in clinical trials.Health Technol Assess1998;2:1-74

[53] Ware JE Jr.Overview of the SF-36 health survey and the international quality of life assessment (IQOLA) project.J Clin Epidemiol1998;51:903-12

[54] Lins L.SF-36 total score as a single measure of health-related quality of life: Scoping review.SAGE Open Med2016;4:2050312116671725 PMCID:PMC5052926

[55] Lee BB,King MT,Marial O.The SF-36 walk-wheel: a simple modification of the SF-36 physical domain improves its responsiveness for measuring health status change in spinal cord injury.Spinal Cord2009;47:50-5

[56] Chung KC,Walters MR.Reliability and validity testing of the michigan hand outcomes questionnaire.J Hand Surg Am1998;23:575-87

[57] Shauver MJ.The Michigan hand outcomes questionnaire after 15 years of field trial.Plast Reconstr Surg2013;131:779e-87e PMCID:PMC3641688

[58] Hudak PL,Bombardier C.Development of an upper extremity outcome measure: the DASH (disabilities of the arm, shoulder, and head).Am J Ind Med1996;29:602-8

[59] Anderson KD,Arp BG.United States (US) multi-center study to assess the validity and reliability of the Spinal Cord Independence Measure (SCIM III).Spinal Cord2011;49:880-5

[60] Catz A.Spinal cord independence measure: comprehensive ability rating scale for the spinal cord lesion patient.J Rehabil Res Dev2007;44:65-8

[61] Rudhe C.Upper extremity function in persons with tetraplegia: relationships between strength, capacity, and the spinal cord independence measure.Neurorehabil Neural Repair2009;23:413-21

[62] Law M,McColl M,Polatajko H.The Canadian occupational performance measure: an outcome measure for occupational therapy.Can J Occup Ther1990;57:82-7

[63] Krasuski M.An analysis of the results of transferring the musculocutaneous nerve onto the median nerve in tetraplegics.Arch Orthop Trauma Surg1991;111:32-3

[64] Anderson KD.Targeting recovery: priorities of the spinal cord-injured population.J Neurotrauma2004;21:1371-83

[65] Lo C,Anderson K,Middleton J.Functional priorities in persons with spinal cord injury: using discrete choice experiments to determine preferences.J Neurotrauma2016;33:1958-68

[66] James MA.Use of the medical research council muscle strength grading system in the upper extremity.J Hand Surg Am2007;32:154-6

[67] Noreau L.Comparison of three methods to assess muscular strength in individuals with spinal cord injury.Spinal Cord1998;36:716-23

[68] Sisto SA.Dynamometry testing in spinal cord injury.J Rehabil Res Dev2007;44:123-36

[69] Berkanovic E,Lachenbruch PA.Concordant and discrepant views of patients' physical functioning.Arthritis Care Res1995;8:94-101

[70] Hewlett SA.Patients and clinicians have different perspectives on outcomes in arthritis.J Rheumatol2003;30:877-9

[71] Szabo RM.Outcomes assessment in hand surgery: when are they meaningful?.J Hand Surg Am2001;26:993-1002

[72] McMillan CR.Which outcome measure is the best? Evaluating responsiveness of the disabilities of the arm, shoulder, and hand questionnaire, the michigan hand questionnaire and the patient-specific functional scale following hand and wrist surgery.Hand2009;4:311-8 PMCID:PMC2724618

[73] Unai K,Takemura R,Liu M.Association between SCIM III total scores and individual item scores to predict independence with ADLS in persons with spinal cord injury.Arch Rehabil Res Clin Transl2019;1:100029 PMCID:PMC7853332

[74] Murphy MA,Sunnerhagen KS.Kinematic variables quantifying upper-extremity performance after stroke during reaching and drinking from a glass.Neurorehabil Neural Repair2011;25:71-80

[75] Bustrén EL,Alt Murphy M.Movement kinematics of the ipsilesional upper extremity in persons with moderate or mild stroke.Neurorehabil Neural Repair2017;31:376-86

[76] Lili L,Rekand T.Associations between upper extremity functioning and kinematics in people with spinal cord injury.J Neuroeng Rehabil2021;18:147 PMCID:PMC8474732

[77] Valevicius AM,Lavoie EB.Characterization of normative hand movements during two functional upper limb tasks.PLoS One2018;13:e0199549 PMCID:PMC6013217