Advertisement
Scientific Article| Volume 46, ISSUE 7, P621.e1-621.e17, July 2021

Evaluation of Functional Independence in Cervical Spinal Cord Injury: Implications for Surgery to Restore Upper Limb Function

Published:January 13, 2021DOI:https://doi.org/10.1016/j.jhsa.2020.10.036

      Purpose

      To help individuals make informed choices regarding the optimal type and timing of restorative surgical treatment for cervical spinal cord injury (SCI), more precise information is needed on their ability to perform activities of daily living. The goal of this work was to describe functional independence achieved by individuals with differing levels of cervical SCI.

      Methods

      Using the comprehensive European Multicenter Study of Spinal Cord Injury dataset, analysis was undertaken of individuals with traumatic SCI, motor-level C5–C8. Data on feeding, bladder management, and transfers (bed to wheelchair) were compared between individuals with different levels of injury. Subgroup analyses of symmetrical and asymmetrical SCI and between complete and incomplete SCI were performed. The impact of age, sex, and time postinjury on functional independence was ascertained.

      Results

      Data were available for individuals with symmetrical (n = 204) and asymmetrical (n = 95) patterns of SCI. Independence with feeding, urinary function, and transfer ability was increased in individuals with strong finger flexion. Unexpectedly, the presence of strong elbow extension did not uniformly result in the ability to transfer independently. There was no change in any of the analyzed activities between 6 and 12 months postinjury.

      Conclusions

      People with cervical SCI who gain finger flexion have greater independence with feeding, urinary, and transfer activities. Restoration of finger flexion should be a reconstructive priority for individuals with midcervical-level SCI.

      Type of study/level of evidence

      Prognostic IV.

      Key words

      Cervical-level spinal cord injury (SCI) causing tetraplegia has a profound impact on upper limb function, affecting activities of daily living (ADLs) and self-care, and it ultimately restricts community integration and quality of life. Approximately 50% of SCI occurs at the cervical level,
      • Wirz M.
      • Dietz V.
      European Multicenter Study of Spinal Cord Injury (EMSCI) Network. Recovery of sensorimotor function and activities of daily living after cervical spinal cord injury: the influence of age.
      with an estimated annual incidence of over 10,000 cases in the United States.
      • Bernhard M1
      • Gries A.
      • Kremer P.
      • Böttiger B.W.
      Spinal cord injury (SCI)—prehospital management.
      Individuals with cervical-level SCI have identified improvement of upper limb function as a top priority.
      • Anderson K.D.
      Targeting recovery: priorities of the spinal cord-injured population.
      ,
      • Snoek G.J.
      • IJzerman M.J.
      • Hermens H.J.
      • Maxwell D.
      • Biering-Sorensen F.
      Survey of the needs of patients with spinal cord injury: impact and priority for improvement in hand function in tetraplegics.
      Peripheral nerve transfer surgeries represent one approach to restoring arm and hand function to increase independence in SCI,
      • Hill E.J.R.
      • Fox I.K.
      Current best peripheral nerve transfers for spinal cord injury.
      • Fox I.K.
      • Davidge K.M.
      • Novak C.B.
      • et al.
      Nerve transfers to restore upper extremity function in cervical spinal cord injury: update and preliminary outcomes.
      • Fox I.K.
      • Davidge K.M.
      • Novak C.B.
      • et al.
      Use of peripheral nerve transfers in tetraplegia: evaluation of feasibility and morbidity.
      • Bertelli J.A.
      • Ghizoni M.F.
      Nerve transfers for restoration of finger flexion in patients with tetraplegia.
      • Bertelli J.A.
      • Ghizoni M.F.
      Transfer of nerve branch to the brachialis to reconstruct elbow extension in incomplete tetraplegia: case report.
      • Bertelli J.A.
      • Ghizoni M.F.
      • Tacca C.P.
      Transfer of the teres minor motor branch for triceps reinnervation in tetraplegia.
      • Bertelli J.A.
      • Tacca C.P.
      • Ghizoni M.F.
      • Kechele P.R.
      • Santos M.A.
      Transfer of supinator motor branches to the posterior interosseous nerve to reconstruct thumb and finger extension in tetraplegia: case report.
      • Fridén J.
      • Gohritz A.
      Brachialis-to-extensor carpi radialis longus selective nerve transfer to restore wrist extension in tetraplegia: case report.
      • Mackinnon S.E.
      • Yee A.
      • Ray W.Z.
      Nerve transfers for the restoration of hand function after spinal cord injury.
      • van Zyl N.
      • Hahn J.B.
      • Cooper C.A.
      • Weymouth M.D.
      • Flood S.J.
      • Galea M.P.
      Upper limb reinnervation in C6 tetraplegia using a triple nerve transfer: case report.
      • van Zyl N.
      • Hill B.
      • Cooper C.
      • Hahn J.
      • Galea M.P.
      Expanding traditional tendon-based techniques with nerve transfers for the restoration of upper limb function in tetraplegia: a prospective case series.
      • Hill E.J.R.
      • Fox I.K.
      Nerve transfers to restore upper limb function in tetraplegia.
      • Khalifeh J.M.
      • Dibble C.F.
      • Van Voorhis A.
      • et al.
      Nerve transfers in the upper extremity following cervical spinal cord injury. Part 2: preliminary results of a prospective clinical trial.
      have been shown to be safe,
      • Fox I.K.
      • Davidge K.M.
      • Novak C.B.
      • et al.
      Nerve transfers to restore upper extremity function in cervical spinal cord injury: update and preliminary outcomes.
      ,
      • Fox I.K.
      • Davidge K.M.
      • Novak C.B.
      • et al.
      Use of peripheral nerve transfers in tetraplegia: evaluation of feasibility and morbidity.
      and require less postoperative immobilization than other reconstructive options such as tendon transfers.

      Hoben H, Varmun R, James A, et al. Nerve transfers to restore and function in cervical level spinal cord injury: a more appealing and accessible option for patients. Paper presented at: American Society for Peripheral Nerve Annual Meeting; January 23-25, 2015; Paradise Island, Bahamas. Abstract 113.

      Candidacy for nerve transfers can be time-sensitive owing to peripheral axon and muscle degeneration from the varying degree of direct lower motor neuron destruction that occurs.
      • Coulet B.
      • Allieu Y.
      • Chammas M.
      Injured metamere and functional surgery of the tetraplegic upper limb.
      ,
      • Fox I.K.
      • Novak C.B.
      • Krauss E.M.
      • et al.
      The use of nerve transfers to restore upper extremity function in cervical spinal cord injury.
      In addition, nerve transfer success may diminish if performed beyond 1 year after SCI,
      • Fu S.Y.
      • Gordon T.
      Contributing factors to poor functional recovery after delayed nerve repair: prolonged denervation.
      ,
      • Kobayashi J.
      • Mackinnon S.E.
      • Watanabe O.
      • et al.
      The effect of duration of muscle denervation on functional recovery in the rat model.
      making timely and informed surgical decision making critically important.
      Gains in motor levels and functional independence occur during rehabilitation, and individuals with motor-incomplete SCI may recover owing to the reorganization of preserved (undamaged) central neural pathways.
      • Raineteau J.
      • Schwab M.E.
      Plasticity of motor systems after incomplete spinal cord injury.
      The degree of this motor recovery, however, is highly variable,
      • Kramer J.L.
      • Lammertse D.P.
      • Schubert M.
      • Curt A.
      • Steeves J.D.
      Relationship between motor recovery and independence after sensorimotor-complete cervical spinal cord injury.
      ,
      • Steeves J.
      • Lammertse D.
      • Kramer J.
      • et al.
      Outcome measures for acute/subacute cervical sensorimotor complete (AIS-A) spinal cord injury during a phase 2 clinical trial.
      and depends on a variety of factors, including the level of SCI, the severity (completeness) of the cord injury,
      • Dietz V.
      • Curt A.
      Neurological aspects of spinal-cord repair: promises and challenges.
      • Kirshblum S.
      • Botticello A.
      • Lammertse D.P.
      • Marino R.J.
      • Chiodo A.E.
      • Jha A.
      The impact of sacral sensory sparing in motor complete spinal cord injury.
      • Denis A.R.
      • Feldman D.
      • Thompson C.
      • Mac-Thiong J.M.
      Prediction of functional recovery six months following traumatic spinal cord injury during acute care hospitalization.
      • Kirshblum S.
      Rehabilitation of spinal cord injury.
      time to spinal cord decompression and stabilization surgery,
      • Jug M.
      • Kejžar N.
      • Vesel M.
      • et al.
      Neurological recovery after traumatic cervical spinal cord injury is superior if surgical decompression and instrumented fusion are performed within 8 hours versus 8 to 24 hours after injury: a single center experience.
      ,
      • Grassner L.
      • Wutte C.
      • Klein B.
      • et al.
      Early decompression (< 8 h) after traumatic cervical spinal cord injury improves functional outcome as assessed by spinal cord independence measure after one year.
      concomitant medical complications following injury,
      • Denis A.R.
      • Feldman D.
      • Thompson C.
      • Mac-Thiong J.M.
      Prediction of functional recovery six months following traumatic spinal cord injury during acute care hospitalization.
      the degree of spinal motor neuron damage,
      • Dietz V.
      • Curt A.
      Neurological aspects of spinal-cord repair: promises and challenges.
      body mass index,
      • Denis A.R.
      • Feldman D.
      • Thompson C.
      • Mac-Thiong J.M.
      Prediction of functional recovery six months following traumatic spinal cord injury during acute care hospitalization.
      and age.
      • Furlan J.C.
      • Fehlings M.G.
      The impact of age on mortality, impairment, and disability among adults with acute traumatic spinal cord injury.
      • Wilson J.R.
      • Grossman R.G.
      • Frankowski R.F.
      • et al.
      A clinical prediction model for long-term functional outcome after traumatic spinal cord injury based on acute clinical and imaging factors.
      • Wilson J.R.
      • Davis A.M.
      • Kulkarni A.V.
      • et al.
      Defining age-related differences in outcome after traumatic spinal cord injury: analysis of a combined, multicenter dataset.
      • Cifu D.X.
      • Seel R.T.
      • Kreutzer J.S.
      • Marwitz J.
      • McKinley W.O.
      • Wisor D.
      Age, outcome and rehabilitation costs after tetraplegia spinal cord injury.
      • Scivoletto G.
      • Morganti B.
      • Molinari M.
      Neurologic recovery of spinal cord injury patients in Italy.
      To add further complexity, a variety of patient factors have a negative impact on ADLs performance, such as increased age,
      • Jug M.
      • Kejžar N.
      • Vesel M.
      • et al.
      Neurological recovery after traumatic cervical spinal cord injury is superior if surgical decompression and instrumented fusion are performed within 8 hours versus 8 to 24 hours after injury: a single center experience.
      ,
      • Jakob W.
      • Wirz M.
      • van Hedel H.J.
      • Dietz V.
      Difficulty of elderly SCI subjects to translate motor recovery—’’body function’’—into daily living activities.
      ,
      • Petland W.
      • McColl M.A.
      • Rosenthal C.
      The effect of aging and duration of disability on long term health outcomes following spinal cord injury.
      autonomic dysreflexia,
      • Nott M.T.
      • Baguley I.J.
      • Heriseanu R.
      • et al.
      Effects of concomitant spinal cord injury and brain injury on medical and functional outcomes and community participation.
      concomitant brain injury,
      • Osterthun R.
      • Tjalma T.A.
      • Spijkerman D.C.M.
      • et al.
      Functional independence of persons with long-standing motor complete spinal cord injury in the Netherlands.
      and the presence of comorbidities.
      • Nott M.T.
      • Baguley I.J.
      • Heriseanu R.
      • et al.
      Effects of concomitant spinal cord injury and brain injury on medical and functional outcomes and community participation.
      Therefore, for a given motor level of injury, there is a range of possible functional independence. Overall, there are paucity of published data on the expected degree of ADLs independence for a given cervical spinal motor level.
      • Steeves J.
      • Lammertse D.
      • Kramer J.
      • et al.
      Outcome measures for acute/subacute cervical sensorimotor complete (AIS-A) spinal cord injury during a phase 2 clinical trial.
      ,
      • Wilson J.R.
      • Grossman R.G.
      • Frankowski R.F.
      • et al.
      A clinical prediction model for long-term functional outcome after traumatic spinal cord injury based on acute clinical and imaging factors.
      ,
      • Schönherr M.C.
      • Groothoff J.W.
      • Mulder G.A.
      • Eisma W.H.
      Prediction of functional outcome after spinal cord injury: a task for the rehabilitation team and the patient.
      The aim of this study was to define improvements in functional independence within the first year after SCI involving motor levels C5 to C8. The primary objective was to establish the relative degree of recovery in functional independence across different motor levels of cervical SCI. The secondary objectives were to determine how functional independence differs between symmetrical and asymmetrical and between complete and incomplete SCI as well as to assess the impact of age, sex, and time postinjury on functional independence. The ultimate goal of this research was to guide decision-making involving early restorative hand surgery, particularly for time-dependent nerve transfers.

      Methods

      European Multicenter Study of Spinal Cord Injury Database

      This database includes deidentified prospectively collected data acquired by the SCI rehabilitation centers participating in the European Multicenter Study of Spinal Cord Injury (EMSCI) study group (www.emsci.org, ClinicalTrials.gov Identifier NCT01571531).
      • Curt A.
      • Schwab M.E.
      • Dietz V.
      Providing the clinical basis for new interventional therapies: refined diagnosis and assessment of recovery after spinal cord injury.
      Institutional review board approval was obtained at the individual SCI centers participating in EMSCI. The database includes individuals’ neurological and functional independence measurements over time. Within the EMSCI network, trained examiners using a uniform protocol assess participants within 2 weeks of initial SCI and subsequently at 1, 3, 6, and 12 months. Neurological assessments are performed according to the International Standards for Neurological Classification of Spinal Cord Injury (ISNCSCI),
      • Kirshblum S.
      • Waring III, W.
      Updates for the International Standards for Neurological Classification of Spinal Cord Injury.
      and include motor and sensory scoring of individual spinal cord segments. Upper extremity motor scores are based on muscle strength scores (Medical Research Council [MRC] 0–5) derived from manual muscle testing of the following key functions deriving primary innervation from a specific spinal cord segment: (1) elbow flexion (C5), (2) wrist extension (C6), (3) elbow extension (C7), (4) finger flexion (C8), and (5) finger abduction (T1).
      • Marino R.J.
      • Barros T.
      • Biering-Sorensen F.
      • et al.
      International standards for neurological classification of spinal cord injury.
      Functional assessments of ADLs (functional independence) are measured using the Spinal Cord Independence Measure (SCIM). This validated performance measure
      • Kramer J.L.
      • Lammertse D.P.
      • Schubert M.
      • Curt A.
      • Steeves J.D.
      Relationship between motor recovery and independence after sensorimotor-complete cervical spinal cord injury.
      ,
      • Catz A.
      • Itzkovich M.
      • Agranov E.
      • Ring H.
      • Tamir A.
      SCIM—spinal cord independence measure: a new disability scale for patients with spinal cord lesions.
      requires direct observation and scoring of the individual performing activities such as feeding, accomplishing urinary function, and transferring from bed to wheelchair.
      • Catz A.
      • Itzkovich M.
      • Agranov E.
      • Ring H.
      • Tamir A.
      SCIM—spinal cord independence measure: a new disability scale for patients with spinal cord lesions.
      ,
      • Anderson K.D.
      • Acuff M.E.
      • Arp B.G.
      • et al.
      United States (US) multi-center study to assess the validity and reliability of the Spinal Cord Independence Measure (SCIM III).
      Demographic data are also collected.

      Data collection

      This study examined the relationship between upper extremity movement and the ability to independently perform feeding, urinary, and transfer activities as captured by the SCIM
      • Catz A.
      • Itzkovich M.
      • Agranov E.
      • Ring H.
      • Tamir A.
      SCIM—spinal cord independence measure: a new disability scale for patients with spinal cord lesions.
      • Anderson K.D.
      • Acuff M.E.
      • Arp B.G.
      • et al.
      United States (US) multi-center study to assess the validity and reliability of the Spinal Cord Independence Measure (SCIM III).
      • Itzkovich M.
      • Gelernter I.
      • Biering-Sorensen F.
      • et al.
      The Spinal Cord Independence Measure (SCIM) version III: reliability and validity in a multi-center international study.
      survey. A query of the central EMSCI database was performed to identify specific data subsets from individuals at 6 months following injury with motor levels C5, C6, C7, or C8 (as determined later under Determining motor level). Age at time of injury, sex, mechanism of injury, and grade (A–D) from the American Spinal Injury Association (ASIA) Impairment Scale (AIS) were collected. For each level of injury, SCIM items 1 (Feeding), 6 (Sphincter Management—Bladder), and 10 (Transfers: Bed-Wheelchair) were recorded at 6 months and 12 months after injury (Fig. 1). The SCIM collects data on a broad range of functional activities including respiratory and other functions. We chose to collect data on activities that individuals with midcervical SCI specifically identified in a previous study
      • Fox I.
      • Hoben G.
      • Komaie G.
      • et al.
      Nerve transfer surgery in cervical spinal cord injury: a qualitative study exploring surgical and caregiver participant experiences [published online ahead of print September 27, 2019]. Disabil Rehabil.
      as relevant to gains in function that can be achieved with surgery. Individuals with incomplete data were excluded from the analysis.
      Figure thumbnail gr1
      Figure 1Spinal Cord Independence Measure (SCIM) items 1 (Feeding), 6 (Sphincter Management—Bladder), and 10 (Transfers: bed—wheelchair). One item from each domain (self-care, sphincter management, mobility) was chosen to widely reflect functional differences at various cervical spinal cord levels. Standardized SCIM answer choices were grouped into independent (green), partial assist (yellow), or full assist (red) as shown.

      Determining motor level

      For this study, C5 motor-level SCI was defined as having elbow flexion MRC grade 3, 4, or 5 with caudal levels C6–T1 as having an MRC grade 0, 1, or 2. Similarly, C6 motor-level SCI was defined as having wrist extension of MRC grade 3, 4, or 5 with caudal levels C7–T1 of MRC grade 0, 1, or 2; C7 motor level was defined as having elbow extension of MRC grade 3, 4, or 5 with caudal levels C8–T1 of MRC grade 0, 1, or 2; and C8 motor level was defined as having finger flexion of MRC grade 3, 4, or 5 with T1 of MRC grade of 0, 1, or 2. All segments rostral to the motor level must have achieved an MRC grade of 4 or 5 or a normal sensory score at C4 where there is no testable motor score available; a normal segmental sensory score (2 of 2) infers a normal C4 segmental motor status. This purposely deviates from how motor level is typically defined by SCI clinicians using the ISNCSCI, in which the motor level is the first spinal segment (indexed by the key muscle group for that segment) having a muscle strength score of at least 3 of 5 (full range contraction against gravity alone), providing all rostral key muscle segmental motor scores are normal (5 of 5).
      • Kramer J.L.
      • Lammertse D.P.
      • Schubert M.
      • Curt A.
      • Steeves J.D.
      Relationship between motor recovery and independence after sensorimotor-complete cervical spinal cord injury.
      As surgeons, we deliberately chose a more inclusive and conservative approach to defining the surgically relevant motor level, where more rostral levels may have muscle strength scores of MRC 4 or 5. Injury patterns were categorized into symmetrical and asymmetrical SCI, with asymmetrical SCI defined as 1 or more motor level difference between sides. Asymmetrical patterns of injury were categorized according to the more caudal level (ie, a person with a C5 motor level on one side and a C7 motor level on the contralateral side was classified as a C7 level injury).

      Range of SCIM activities

      The range of performance for each of the 3 SCIM activity items was examined and correlated with the individual’s motor level. The SCIM item scores were condensed by the authors into independent, partial assist, and full assist as shown in Figure 1. Range of functional independence between 6 and 12 months was compared to see whether there were changes in functional activity with greater time following injury. Subgroup analyses were performed between symmetrical and asymmetrical injuries, as well as motor-complete (ASIA A, B) and motor-incomplete (ASIA C, D) injury patterns. The impact of age (categorized as <40, 40–60, or >60 years), sex, time since injury, and degree of asymmetry (for asymmetrical SCI, number of intervening levels) on independence was ascertained.

      Statistical analysis

      Descriptive statistics were used to summarize baseline characteristics. The SCIM item scores at each motor level were reported with 95% confidence intervals. The Fisher exact test was used to compare SCIM scores for a given motor level among the following groups: (1) 6 versus 12 months after SCI, (2) symmetrical versus asymmetrical SCI, and (3) motor-complete (ASIA A or B) versus motor-incomplete (ASIA C or D) patterns of injury. The impact of age, sex, and degree of asymmetry on SCIM scores was also evaluated using Fisher exact test.

      Results

      There were 299 individuals with motor level C5 to C8 spinal cord injury at 6 months included in this study; 204 (68%) had symmetrical SCI, and 95 (32%) had asymmetrical patterns of SCI. Demographic characteristics for the symmetrical and asymmetrical groups were similar (mean age, 42 ± 18 years; 81% male; Table 1). The most common cause of SCI was trauma (97%), followed by ischemia (3%). The AIS category was distributed as follows: AIS A 47%, AIS B 25%, AIS C 19%, and AIS D 9%. Motor level was distributed as follows: C5 28% (n = 85), C6 38% (n = 113), C7 23% (n = 68), and C8 11% (n = 33).
      Table 1Demographic Data, SCI Motor Level C5–C8
      Asymmetrical pattern of injury was defined as 1 or more motor level difference between sides. AIS category is defined as A complete, B sensory incomplete, C motor-incomplete with > 50% of key muscles below the level graded as MRC < 3, and D motor-incomplete with > 50% of key muscles below the level graded as MRC ≥ 3. Motor levels were assigned based on the most cephalad level at which MRC was graded 3, 4, or 5 with all rostral levels 4 or 5 and all caudal levels 0, 1, or 2. Motor level is defined as the most caudal level at which the MRC grade is 3, 4, or 5.
      Symmetrical n = 204Asymmetrical n = 95
      Age, y (mean ± SD)41 ± 1844 ± 18
      Sex, n (%)Male 163 (80)Male 79 (83)
      Female 41 (20)Female 16 (17)
      Mechanism of injury, n (%)Traumatic 198 (97) Ischemic 6 (4)Traumatic 91 (96) Ischemic 4 (4)
      AIS category, n (%)AIS A 94 (48)AIS A 40 (44)
      AIS B 50 (25)AIS B 23 (25)
      AIS C 34 (17)AIS C 22 (24)
      AIS D 19 (10)AIS D 6 (7)
      Motor level, n (%)C5 58 (28)C5 27 (28)
      Motor level on the more caudal side.
      C6 83 (41)C6 30 (32)
      Motor level on the more caudal side.
      C7 44 (22)C7 24 (25)
      Motor level on the more caudal side.
      C8 19 (9)C8 14 (15)
      Motor level on the more caudal side.
      AIS, American Spinal Injury Association Impairment Scale.
      Asymmetrical pattern of injury was defined as 1 or more motor level difference between sides. AIS category is defined as A complete, B sensory incomplete, C motor-incomplete with > 50% of key muscles below the level graded as MRC < 3, and D motor-incomplete with > 50% of key muscles below the level graded as MRC ≥ 3. Motor levels were assigned based on the most cephalad level at which MRC was graded 3, 4, or 5 with all rostral levels 4 or 5 and all caudal levels 0, 1, or 2. Motor level is defined as the most caudal level at which the MRC grade is 3, 4, or 5.
      Motor level on the more caudal side.

      Feeding capacity

      The range of functional independence in feeding (SCIM item 1) by motor level is shown in Figure 2 for symmetrical SCI and Figure E1 for asymmetrical SCI. Corresponding confidence intervals for all activities are shown in Table 2 and Table E1. Functional independence in feeding for symmetrical SCI is further broken down into motor-complete and motor-incomplete injury in Figure E2. Feeding requiring personal assistance or adaptive devices was found for the majority of patients with MRC 3 to 5 wrist extension (C6 motor level), which enables use of tenodesis-driven hand function. Feeding independently without need for assistance or adaptive devices was found for individuals with the added function of MRC grade 3 to 5 finger flexion (C8 motor level). Independence with feeding did not change between 6 and 12 months at any injury level. Subgroup analysis showed that individuals with C6 motor level were more independent in feeding if they were younger (<40 versus >60 years). No association of sex, AIS category, or magnitude of asymmetry with independence with feeding was found.
      Figure thumbnail gr2
      Figure 2Feeding (SCIM item 1) by motor level for symmetrical SCI, 6 months and 12 months after injury. Data are presented as percentage of the total. Feeding with assistance or adaptive devices was noted for the majority with strong (MRC 3–5) wrist extension (C6 function). Feeding independently without need for assistance or adaptive devices was noted only for individuals with strong (MRC 3–5) wrist flexion (C8 function). A trend toward greater independence with greater time postinjury was seen.
      Table 2Distribution of Independence With Feeding, Bladder Management, and Transfers (Bed to Wheelchair) for Motor Levels C5–C8 Symmetrical SCI, 6 Months, and 12 Months After Injury, as Assessed by SCIM (Items 1, 6, 10, Respectively)
      Data are presented as percentage of the total with 95% confidence intervals. Six-mo data for all patients are presented in addition to 6-mo data for only those with corresponding 12-mo data available (bold). Numbers in parentheses (n) correspond to SCIM scores.
      FeedingMotor LevelTime (mo)nDistribution of Level of Independence With 95% Confidence Intervals (%)
      Full Assist (0)Partial Assistance or Adaptive Device (1–2)Independent (3)
      C565841 ± 1359 ± 130
      63238 ± 1763 ± 170
      123234 ± 1666 ± 160
      C668312 ± 888 ± 80
      65613 ± 988 ± 90
      12564 ± 595 ± 62 ± 4
      C76442 ± 495 ± 62 ± 4
      6313 ± 697 ± 60
      12313 ± 690 ± 116 ± 8
      C86195 ± 1053 ± 2242 ± 22
      6119 ± 1736 ± 2855 ± 29
      1211045 ± 2955 ± 29
      Bladder ManagementMotor LevelTime (mo)nRequires Assist (0, 3, 6)Independent (9, 11, 13, 15)
      C56581000
      6321000
      123297 ± 63 ± 6
      C668393 ± 57 ± 5
      65693 ± 77 ± 7
      125686 ± 914 ± 9
      C764475 ± 1325 ± 13
      63171 ± 1629 ± 16
      123168 ± 1632 ± 16
      C861947 ± 2253 ± 22
      61127 ± 2673 ± 26
      121127 ± 2673 ± 26
      TransfersMotor LevelTime (mo)nFull Assist (0)Partial Assistance or Adaptive Device (1)Independent (2)
      C565891 ± 79 ± 70
      63288 ± 1112 ± 110
      123288 ± 119 ± 103 ± 6
      C668376 ± 919 ± 85 ± 5
      65675 ± 1121 ± 114 ± 5
      125659 ± 1329 ± 1213 ± 9
      C764445 ± 1534 ± 1420 ± 12
      63145 ± 1835 ± 1719 ± 14
      124135 ± 1745 ± 1819 ± 14
      C861916 ± 1647 ± 2237 ± 22
      6119 ± 1736 ± 2855 ± 29
      121118 ± 2318 ± 2364 ± 28
      Data are presented as percentage of the total with 95% confidence intervals. Six-mo data for all patients are presented in addition to 6-mo data for only those with corresponding 12-mo data available (bold). Numbers in parentheses (n) correspond to SCIM scores.

      Bladder management

      Range of functional independence in bladder management (SCIM item 6) by motor level is shown in Figure 3 for symmetrical SCI and Figure E3 for asymmetrical SCI. Corresponding confidence intervals for all activities are shown in Table 2 and Table E1. Functional independence in bladder management for symmetrical SCI is further broken down into motor-complete and motor-incomplete injury in Figure E4. Independence with bladder management was found in those with MRC 3 to 5 finger flexion (C8 motor level). Independence with bladder management did not change between 6 and 12 months at any injury level. Subgroup analysis showed that individuals were more independent in bladder management at the C6 level if they had some trunk or lower extremity control (motor-incomplete injuries). No association of age, sex, or magnitude of asymmetry on independence with bladder management was found.
      Figure thumbnail gr3
      Figure 3Bladder management (SCIM item 6) by motor level for symmetrical SCI, 6 months and 12 months after injury. Data are presented as percentage of the total. Independence with bladder management was noted in those with strong (MRC 3–5) finger flexion (C8 function). A trend toward greater independence with greater time postinjury was seen.

      Transfers (bed to wheelchair)

      Range of functional independence in transfers, bed to wheelchair (SCIM item 10) by motor level is shown in Figure 4 for symmetrical SCI and Figure E5 for asymmetrical SCI. Corresponding confidence intervals for all activities are shown in Table 2 and Table E1. Functional independence in transfers for symmetrical SCI is further broken down into motor-complete and motor-incomplete injury in Figure E6. The MRC 3- to 5 elbow extension (C7 motor level) did not uniformly result in the ability to transfer independently; only 54% to 64% of individuals with elbow extension were independent in transfers. Subgroup analysis showed that individuals with stronger elbow extension (MRC 5 > 4 > 3) had equivalent independence with transfers. The addition of MRC 3 to 5 finger flexion (C8 motor level), however, was associated with greater independence with transfers. Of note, a small subset of individuals (5%–13%) were able to transfer independently even without any elbow extension movement. Independence with transfers did not change between 6 and 12 months after injury. Subgroup analysis showed that individuals were more independent with transfers at the C6 level if they were younger or at the C5, C6, or C7 level if they had trunk or lower extremity control (motor-incomplete injuries). No association of sex or magnitude of asymmetry on independence with transfers was found.
      Figure thumbnail gr4
      Figure 4Transfers, bed to wheelchair (SCIM item 10), by motor level for symmetrical SCI, 6 months and 12 months after injury. Data are presented as percentage of the total. Strong (MRC 3–5) elbow extension (C7 function) did not uniformly result in the ability to transfer independently; only 20% of individuals with intact elbow extension were independent in transfers at 6 months. Strong (MRC 3–5) finger flexion (C8 function), however, was noted to be present in those who were independent with transfers. Notably, these data also show that a small subset of 5% to13% of individuals is able to transfer without any elbow extension present (C6 level). A trend toward greater independence with greater time postinjury was seen.

      Discussion

      The inherent heterogeneity of SCI
      • Steeves J.
      • Lammertse D.
      • Kramer J.
      • et al.
      Outcome measures for acute/subacute cervical sensorimotor complete (AIS-A) spinal cord injury during a phase 2 clinical trial.
      ,
      • Dietz V.
      • Curt A.
      Neurological aspects of spinal-cord repair: promises and challenges.
      renders prediction of independence with self-care challenging,
      • Fox I.
      • Hoben G.
      • Komaie G.
      • et al.
      Nerve transfer surgery in cervical spinal cord injury: a qualitative study exploring surgical and caregiver participant experiences [published online ahead of print September 27, 2019]. Disabil Rehabil.
      and little has been published on this subject.
      • Steeves J.
      • Lammertse D.
      • Kramer J.
      • et al.
      Outcome measures for acute/subacute cervical sensorimotor complete (AIS-A) spinal cord injury during a phase 2 clinical trial.
      ,
      • Wilson J.R.
      • Grossman R.G.
      • Frankowski R.F.
      • et al.
      A clinical prediction model for long-term functional outcome after traumatic spinal cord injury based on acute clinical and imaging factors.
      ,
      • Krishna V.
      • Andrews H.
      • Varma A.
      • Mintzer J.
      • Kindy M.
      • Guest J.
      Spinal cord injury: how can we improve the classification and quantification of its severity and prognosis?.
      Our study provides some information on the functional independence levels for specific ADLs in individuals with cervical SCI at motor levels C5 to C8 at 6 and 12 months after injury. This knowledge can guide expectations on independence after SCI and can be used to inform individuals with SCI and clinicians on decision-making around early restorative upper limb surgery.
      Individuals with acute SCI must process an overwhelming amount of information during rehabilitation to resume daily activities and maintain health. This includes modification of mobility, bladder and bowel function, pressure-offloading, and spasticity management. The transition from inpatient rehabilitation to home requires careful planning and coordinated care. Knowledge of the time course of expected functional recovery and attainable levels of independence is important to inform decisions about rehabilitation and participation in potential therapeutic interventions.
      Previous studies have examined target values for SCIM scoring at various neurological levels
      • Aidinoff E.
      • Front L.
      • Itzkovich M.
      • et al.
      Expected spinal cord independence measure, third version, scores for various neurological levels after complete spinal cord lesions.
      or in tetraplegia as a whole.
      • Rudhe C.
      • van Hedel H.J.
      Upper extremity function in persons with tetraplegia: relationships between strength, capacity, and the spinal cord independence measure.
      Published guidelines on expected independence 1 year after injury suggest that feeding with adaptive devices is possible with a C5 motor level and independence with feeding requires a C7 motor level.
      • Kirshblum S.C.
      • Bloomgarden J.
      • Nead C.
      • McClure I.
      • Forrest G.
      • Mitchell J.
      Rehabilitation of spinal cord injury.
      By contrast, the results presented here suggest that feeding with assistive devices requires a strong wrist extension, and full independence requires strong finger flexion. Greater independence with bladder management also required strong finger flexion. Published guidelines suggest independence with transfers is possible for those with a C7 (elbow extension) motor level.
      • Kirshblum S.C.
      • Bloomgarden J.
      • Nead C.
      • McClure I.
      • Forrest G.
      • Mitchell J.
      Rehabilitation of spinal cord injury.
      This study, by contrast, showed that strong C8 motor scores were better associated with independence in transfers. Physiologically, this makes sense as the addition of C8-driven grasp of the wheelchair arm-to-body support by use of elbow extension together contribute to transfer ability. Subgroup analyses showed the impact of age, sex, and degree of motor completeness (AIS category) on independence. Previous studies have also shown that lower functional independence is associated with increased age
      • Jug M.
      • Kejžar N.
      • Vesel M.
      • et al.
      Neurological recovery after traumatic cervical spinal cord injury is superior if surgical decompression and instrumented fusion are performed within 8 hours versus 8 to 24 hours after injury: a single center experience.
      ,
      • Wilson J.R.
      • Grossman R.G.
      • Frankowski R.F.
      • et al.
      A clinical prediction model for long-term functional outcome after traumatic spinal cord injury based on acute clinical and imaging factors.
      ,
      • Wilson J.R.
      • Davis A.M.
      • Kulkarni A.V.
      • et al.
      Defining age-related differences in outcome after traumatic spinal cord injury: analysis of a combined, multicenter dataset.
      ,
      • Jakob W.
      • Wirz M.
      • van Hedel H.J.
      • Dietz V.
      Difficulty of elderly SCI subjects to translate motor recovery—’’body function’’—into daily living activities.
      ,
      • Petland W.
      • McColl M.A.
      • Rosenthal C.
      The effect of aging and duration of disability on long term health outcomes following spinal cord injury.
      and motor-complete injuries,
      • Denis A.R.
      • Feldman D.
      • Thompson C.
      • Mac-Thiong J.M.
      Prediction of functional recovery six months following traumatic spinal cord injury during acute care hospitalization.
      ,
      • Kirshblum S.C.
      • Bloomgarden J.
      • Nead C.
      • McClure I.
      • Forrest G.
      • Mitchell J.
      Rehabilitation of spinal cord injury.
      ,
      • Kalsi-Ryan S.
      • Beaton D.
      • Curt A.
      • Popovic M.R.
      • Verrier M.C.
      • Fehlings M.G.
      Outcome of the upper limb in cervical spinal cord injury: profiles of recovery and insights for clinical studies.
      whereas other studies have shown no effect of age on SCIM scores.
      • Kaminski L.
      • Cordemans V.
      • Cernat E.
      • M’Bra K.I.
      • Mac-Thiong J.M.
      Functional outcome prediction after traumatic spinal cord injury based on acute clinical factors.
      In our study, we did see some effect of age on feeding and transfer activities.
      Increased independence with activities is not only highly desired by individuals with SCI, it can also reduce caregiver cost and burden. Both tendon
      • Hentz V.R.
      • LeClercq C.
      Surgical Rehabilitation of the Upper Limb in Tetraplegia.
      and nerve transfer surgery can restore a variety of upper limb functions including hand closing and opening, which this work shows is critical to independent feeding, urinary, and transfer function. Unfortunately, as few as 14% of eligible individuals receive upper limb surgery in the United States.
      • Curtin C.M.
      • Gater D.R.
      • Chung K.C.
      Upper extremity reconstruction in the tetraplegic population, a national epidemiologic study.
      Depending on the level of injury and available intact donor nerves, nerve transfers have been used to restore a variety of functions. These include wrist extension,
      • Fridén J.
      • Gohritz A.
      Brachialis-to-extensor carpi radialis longus selective nerve transfer to restore wrist extension in tetraplegia: case report.
      elbow extension,
      • Bertelli J.A.
      • Ghizoni M.F.
      • Tacca C.P.
      Transfer of the teres minor motor branch for triceps reinnervation in tetraplegia.
      ,
      • Bertelli J.A.
      • Ghizoni M.F.
      Nerve transfers for elbow and finger extension reconstruction in midcervical spinal cord injuries.
      finger flexion,
      • Bertelli J.A.
      • Ghizoni M.F.
      Nerve transfers for restoration of finger flexion in patients with tetraplegia.
      and finger extension.
      • Bertelli J.A.
      • Tacca C.P.
      • Ghizoni M.F.
      • Kechele P.R.
      • Santos M.A.
      Transfer of supinator motor branches to the posterior interosseous nerve to reconstruct thumb and finger extension in tetraplegia: case report.
      Work on indications, selection, and long-term outcomes of nerve transfers is ongoing. Establishing a neurological plateau prior to nerve transfer is critical because nerve transfer would halt further spontaneous recovery in the recipient muscle(s); however, studies have shown that the results of nerve transfers diminish when surgery is done further from time of injury.
      • van Zyl N.
      • Hill B.
      • Cooper C.
      • Hahn J.
      • Galea M.P.
      Expanding traditional tendon-based techniques with nerve transfers for the restoration of upper limb function in tetraplegia: a prospective case series.
      ,
      • Cain S.A.
      • Gohritz A.
      • Fridén J.
      • van Zyl N.
      Review of upper extremity nerve transfer in cervical spinal cord injury.
      Tendon transfers can similarly restore elbow extension, hand opening and closing, and other functions. Although from a physiological standpoint, tendon transfers may be completed at any time following SCI, some work suggests that people with SCIs may prefer having this surgery within a year of injury.
      • Anderson K.D.
      • Fridén J.
      • Lieber R.L.
      Acceptable benefits and risks associated with surgically improving arm function in individuals living with cervical spinal cord injury.
      Our results showed that there was no change in independence with feeding, bladder management, or transfers between 6 and 12 months after SCI. Additional work by our group shows that few individuals recover additional motor movement between 6 and 12 months: only 3% of individuals without C7 motor function at 6 months gain strong C7 motor function at 12 months, and only 3% without C8 motor function gain strong C8 motor function by 12 months.

      Fox I, Dengler J, Curt A, et al. Degree of upper extremity function recovery in cervical spinal cord injury: implications for peripheral nerve transfer surgery to restore upper limb function. Paper presented at: 58th ISCoS Annual Scientific Meeting; November 5-7, 2019; France.

      This suggests that evaluation for surgical intervention as early as 6 months after SCI could be considered. Previous studies have shown that recovery beyond 12 months is limited (but greater in incomplete tetraplegia).
      • Kirshblum S.
      • Millis S.
      • McKinley W.
      • Tulsky D.
      Late neurologic recovery after traumatic spinal cord injury.
      • Ditunno Jr., J.F.
      • Cohen M.E.
      • Hauck W.W.
      • Jackson A.B.
      • Sipski M.L.
      Recovery of upper-extremity strength in complete and incomplete tetraplegia: a multicenter study.
      • Waters R.L.
      • Adkins R.H.
      • Yakura J.S.
      • Sie I.
      Motor and sensory recovery following complete tetraplegia.
      • Waters R.L.
      • Adkins R.H.
      • Yakura J.S.
      • Sie I.
      Motor and sensory recovery following incomplete tetraplegia.
      Database studies have inherent limitations. The sample size in this study was limited by the data available, missing SCIM scores, and a dropoff in follow-up between 6 and 12 months after SCI; it may have been underpowered. Although no improvements in function were seen, this does not preclude the individual possibility of this occurring. The insights gained from the study should be taken as 1 more data point in a complex decision algorithm for both the provider and the patient. We were also unable to assess other factors that are known to affect independence such as the presence of traumatic brain injury, autonomic dysreflexia, spasticity, and multiple comorbidities,
      • Denis A.R.
      • Feldman D.
      • Thompson C.
      • Mac-Thiong J.M.
      Prediction of functional recovery six months following traumatic spinal cord injury during acute care hospitalization.
      ,
      • Nott M.T.
      • Baguley I.J.
      • Heriseanu R.
      • et al.
      Effects of concomitant spinal cord injury and brain injury on medical and functional outcomes and community participation.
      ,
      • Osterthun R.
      • Tjalma T.A.
      • Spijkerman D.C.M.
      • et al.
      Functional independence of persons with long-standing motor complete spinal cord injury in the Netherlands.
      because these data were not included in the database.
      In addition, the rehabilitation care received by individuals in the EMSCI database may not parallel that of individuals in the United States or other countries. Motor recovery is in part due to strengthening of existing function,
      • Ditunno Jr., J.F.
      • Cohen M.E.
      • Hauck W.W.
      • Jackson A.B.
      • Sipski M.L.
      Recovery of upper-extremity strength in complete and incomplete tetraplegia: a multicenter study.
      and independence in activities is affected by learned behaviors; thus, rehabilitation treatment and motivation can affect functional outcomes.
      • Kramer J.L.
      • Lammertse D.P.
      • Schubert M.
      • Curt A.
      • Steeves J.D.
      Relationship between motor recovery and independence after sensorimotor-complete cervical spinal cord injury.
      ,
      • Catz A.
      • Itzkovich M.
      • Agranov E.
      • Ring H.
      • Tamir A.
      SCIM—spinal cord independence measure: a new disability scale for patients with spinal cord lesions.
      ,
      • Catz A.
      • Greenberg E.
      • Itzkovich M.
      • Bluvshtein V.
      • Ronen J.
      • Gelernter I.
      A new instrument for outcome assessment in rehabilitation medicine: spinal cord injury ability realization measurement index.
      ,
      • Kalsi-Ryan S.
      • Beaton D.
      • Curt A.
      • et al.
      The Graded Redefined Assessment of Strength Sensibility and Prehension (GRASSP): reliability and validity.
      The EMSCI-derived results may overpredict gains in function that would be seen in more-disadvantaged populations with less access to comprehensive and no-cost rehabilitation care.
      The SCIM is focused on observed gains in ability to perform a specific activity (such as feeding) and does not necessarily measure real-life behavior. Accomplishing an activity does not mean completing it as the individual desires. Thus, the SCIM may overestimate the satisfactory level of independence. Finally, the data presented here do not include improvements in functional independence beyond 12 months. In this study, single items from the SCIM were used to determine independence. Whereas the SCIM has been validated, the application of single items may not possess similar high-validity psychometrics. However, these items were chosen to be most relevant for surgeons who evaluate and treat individuals with midcervical SCI.
      Overall, our study shows that spontaneous gains in functional independence start to plateau by 6 months after SCI, and improvements in strength after 6 months were not reflected in functional independence. This should influence decision-making for individuals with SCI and their clinicians when considering intervention to augment function such as nerve and/or tendon transfer.

      Acknowledgments

      The members of the Department of Defense (DOD) group are Catherine Curtin, MD, Palo Alto Veterans Healthcare System, Palo Alto, CA; Carie Kennedy, BSN, RN, Division of Plastic and Reconstructive Surgery, Department of Surgery, Washington University School of Medicine, St. Louis, MO; Amanda Miller, MD, Division of Physical Medicine and Rehabilitation, Washington University School of Medicine, St. Louis, MO; Christine Novak, PhD, Division of Plastic and Reconstructive Surgery, Department of Surgery, University of Toronto, Toronto, Ontario, Canada; Doug Ota, MD, Palo Alto Veterans Healthcare System, Palo Alto, CA; and Katherine C. Stenson, MD, Division of Plastic and Reconstructive Surgery, Department of Surgery, Washington University School of Medicine, St. Louis, MO, and VA St. Louis Healthcare System, St. Louis, MO.
      The members of the EMSCI group are Armin Curt, MD, Spinal Cord Injury Center, Balgrist University Hospital, Zurich, Switzerland; Doris Maier, MD, BG-Trauma Center, Murnau, Germany; Rainer Abel, MD, PhD, Hohe Warte Bayreuth, Bayreuth, Germany; Norbert Weidner, MD, PhD, Rüdiger Rupp, MD, Spinal Cord Injury Center, Heidelberg University Hospital, Heidelberg, Germany; J. Vidal, MD, Institute Guttmann, Neurorehabilitation Hospital, Barcelona, Spain; Jesus Benito, MD, Institute Guttmann, Neurorehabilitation Hospital, Barcelona, Spain; and Yorck-Bernhard Kalke, MD, RKU Universitäts- und Rehabilitationskliniken Ulm, Ulm, Germany.
      IKF grant funding support was provided by the U.S. Department of Defense—Project #W81XWH-17-1-0285 “Supporting Patient Decisions about Upper-Extremity Surgery in Cervical SCI.”
      The contents of this work do not represent the views of the U.S. Department of Veterans Affairs or the U.S. Government.

      Supplementary Data

      Figure thumbnail fx1
      Figure E1Feeding (SCIM item 1) by motor level for asymmetrical SCI, 6 months and 12 months after injury. Data are presented as percentage of the total. Feeding with assistance or adaptive devices was noted for the majority with strong (MRC 3–5) wrist extension (C6 function). Feeding independently without need for assistance or adaptive devices was noted only for individuals with strong (MRC 3–5) wrist flexion (C8 function). A trend toward greater independence with greater time postinjury was seen.
      Figure thumbnail fx2
      Figure E2Feeding (SCIM item 1) by motor level for symmetrical SCI, 6 months and 12 months after injury for motor-complete (ASIA A, B) and motor-incomplete (ASIA C, D; highlighted by blue square). Data are presented as percentage of the total. No difference in the change from 6 to 12 months was seen between the motor-complete and the motor-incomplete groups.
      Figure thumbnail fx3
      Figure E3Bladder management (SCIM item 6) by motor level for asymmetrical SCI, 6 months and 12 months after injury. Data are presented as percentage of the total. Independence with bladder management was noted in those with strong (MRC 3–5) finger flexion (C8 function). A trend toward greater independence with greater time postinjury was seen.
      Figure thumbnail fx4
      Figure E4Bladder management (SCIM item 6) by motor level for symmetrical SCI, 6 months and 12 months after injury for motor-complete (ASIA A, B) and motor-incomplete (ASIA C, D; highlighted by blue square). Data are presented as percentage of the total. No difference in the change from 6 to 12 months was seen between the motor-complete and the motor-incomplete groups.
      Figure thumbnail fx5
      Figure E5Transfers, bed to wheelchair (SCIM item 10), by motor level for asymmetrical SCI, 6 months and 12 months after injury. Data are presented as percentage of the total. Strong (MRC 3–5) elbow extension (C7 function) did not uniformly result in the ability to transfer independently; only 8% of individuals with intact elbow extension were independent in transfers at 6 months. Strong (MRC 3–5) finger flexion (C8 function), however, was noted to be present in those who were independent with transfers. Notably, there data also show that a small subset of 3% to 6% of individuals were able to transfer without any elbow extension present (C6 level). A trend toward greater independence with greater time postinjury was seen.
      Figure thumbnail fx6
      Figure E6Transfers, bed to wheelchair (SCIM item 10), by motor level for symmetrical SCI, 6 months and 12 months after injury for motor-complete (ASIA A, B) and motor-incomplete (ASIA C, D; highlighted by blue square). Data are presented as percentage of the total. No difference in the change from 6 to 12 months was seen between the motor-complete and the motor-incomplete groups.
      Table E1Distribution of Independence With Feeding, Bladder Management, and Transfers (Bed to Wheelchair) for Motor Levels C5–C8 Symmetrical SCI, 6 Months And 12 Months After Injury, as Assessed by SCIM (Items 1, 6, 10, Respectively)
      Data are presented as percentage of the total with 95% confidence intervals. Six-mo data for all patients are presented in addition to 6-mo data for only those with corresponding 12-mo data available (bold). Numbers in parentheses (n) correspond to SCIM scores.
      FeedingMotor LevelTime (mo)nDistribution of Level of Independence With 95% Confidence Intervals (%)
      Full Assist (0)Partial Assistance or Adaptive Device (1–2)Independent (3)
      C562763 ± 1837 ± 180
      61567 ± 2433 ± 240
      121567 ± 2433 ± 240
      C663030 ± 1670 ± 160
      61625 ± 2175 ± 210
      121619 ± 1981 ± 190
      C76244 ± 886 ± 80
      6147 ± 1393 ± 130
      121401000
      C8614093 ± 137 ± 13
      610090 ± 1910 ± 19
      1210060 ± 3040 ± 30
      Bladder ManagementMotor LevelTime (mo)nRequires Assist (0, 3, 6)Independent (9, 11, 13, 15)
      C56271000
      6151000
      12151000
      C663093 ± 97 ± 9
      61694 ± 126 ± 12
      121694 ± 126 ± 12
      C76241000
      6141000
      121486 ± 1814 ± 18
      C861471 ± 2429 ± 24
      61080 ± 25 %20 ± 25 %
      121060 ± 30 %40 ± 30 %
      TransfersMotor LevelTime (mo)nFull Assist (0)Partial Assistance or Adaptive Device (1)Independent (2)
      C562710000
      61510000
      121597 ± 93 ± 90
      C663097 ± 603 ± 6
      61694 ± 1206 ± 12
      121688 ± 166 ± 126 ± 12
      C762467 ± 1925 ± 178 ± 11
      61457 ± 2629 ± 2414 ± 18
      121457 ± 2614 ± 1829 ± 24
      C861436 ± 2536 ± 2529 ± 24
      61040 ± 3020 ± 2540 ± 30
      121030 ± 2830 ± 2840 ± 30
      Data are presented as percentage of the total with 95% confidence intervals. Six-mo data for all patients are presented in addition to 6-mo data for only those with corresponding 12-mo data available (bold). Numbers in parentheses (n) correspond to SCIM scores.

      References

        • Wirz M.
        • Dietz V.
        European Multicenter Study of Spinal Cord Injury (EMSCI) Network. Recovery of sensorimotor function and activities of daily living after cervical spinal cord injury: the influence of age.
        J Neurotrauma. 2015; 32: 194-199
        • Bernhard M1
        • Gries A.
        • Kremer P.
        • Böttiger B.W.
        Spinal cord injury (SCI)—prehospital management.
        Resuscitation. 2005; 66: 127-139
        • Anderson K.D.
        Targeting recovery: priorities of the spinal cord-injured population.
        J Neurotrauma. 2004; 21: 1371-1383
        • Snoek G.J.
        • IJzerman M.J.
        • Hermens H.J.
        • Maxwell D.
        • Biering-Sorensen F.
        Survey of the needs of patients with spinal cord injury: impact and priority for improvement in hand function in tetraplegics.
        Spinal Cord. 2004; 42: 526-532
        • Hill E.J.R.
        • Fox I.K.
        Current best peripheral nerve transfers for spinal cord injury.
        Plast Reconstr Surg. 2019; 143: 184e-198e
        • Fox I.K.
        • Davidge K.M.
        • Novak C.B.
        • et al.
        Nerve transfers to restore upper extremity function in cervical spinal cord injury: update and preliminary outcomes.
        Plast Reconstr Surg. 2015; 136: 780-792
        • Fox I.K.
        • Davidge K.M.
        • Novak C.B.
        • et al.
        Use of peripheral nerve transfers in tetraplegia: evaluation of feasibility and morbidity.
        Hand (N Y). 2015; 10: 60-67
        • Bertelli J.A.
        • Ghizoni M.F.
        Nerve transfers for restoration of finger flexion in patients with tetraplegia.
        J Neurosurg Spine. 2017; 26: 55-61
        • Bertelli J.A.
        • Ghizoni M.F.
        Transfer of nerve branch to the brachialis to reconstruct elbow extension in incomplete tetraplegia: case report.
        J Hand Surg Am. 2012; 37: 1990-1993
        • Bertelli J.A.
        • Ghizoni M.F.
        • Tacca C.P.
        Transfer of the teres minor motor branch for triceps reinnervation in tetraplegia.
        J Neurosurg. 2011; 114: 1457-1460
        • Bertelli J.A.
        • Tacca C.P.
        • Ghizoni M.F.
        • Kechele P.R.
        • Santos M.A.
        Transfer of supinator motor branches to the posterior interosseous nerve to reconstruct thumb and finger extension in tetraplegia: case report.
        J Hand Surg Am. 2010; 35: 1647-1651
        • Fridén J.
        • Gohritz A.
        Brachialis-to-extensor carpi radialis longus selective nerve transfer to restore wrist extension in tetraplegia: case report.
        J Hand Surg Am. 2012; 37: 1606-1608
        • Mackinnon S.E.
        • Yee A.
        • Ray W.Z.
        Nerve transfers for the restoration of hand function after spinal cord injury.
        J Neurosurg. 2012; 117: 176-185
        • van Zyl N.
        • Hahn J.B.
        • Cooper C.A.
        • Weymouth M.D.
        • Flood S.J.
        • Galea M.P.
        Upper limb reinnervation in C6 tetraplegia using a triple nerve transfer: case report.
        J Hand Surg Am. 2014; 39: 1779-1783
        • van Zyl N.
        • Hill B.
        • Cooper C.
        • Hahn J.
        • Galea M.P.
        Expanding traditional tendon-based techniques with nerve transfers for the restoration of upper limb function in tetraplegia: a prospective case series.
        Lancet. 2019; 394: 565-575
        • Hill E.J.R.
        • Fox I.K.
        Nerve transfers to restore upper limb function in tetraplegia.
        Lancet. 2019; 394: 543-544
        • Khalifeh J.M.
        • Dibble C.F.
        • Van Voorhis A.
        • et al.
        Nerve transfers in the upper extremity following cervical spinal cord injury. Part 2: preliminary results of a prospective clinical trial.
        J Neurosurg Spine. 2019; 31: 619-773
      1. Hoben H, Varmun R, James A, et al. Nerve transfers to restore and function in cervical level spinal cord injury: a more appealing and accessible option for patients. Paper presented at: American Society for Peripheral Nerve Annual Meeting; January 23-25, 2015; Paradise Island, Bahamas. Abstract 113.

        • Coulet B.
        • Allieu Y.
        • Chammas M.
        Injured metamere and functional surgery of the tetraplegic upper limb.
        Hand Clin. 2002; 18: 399-412
        • Fox I.K.
        • Novak C.B.
        • Krauss E.M.
        • et al.
        The use of nerve transfers to restore upper extremity function in cervical spinal cord injury.
        PM R. 2018; 10: 1173-1184.e2
        • Fu S.Y.
        • Gordon T.
        Contributing factors to poor functional recovery after delayed nerve repair: prolonged denervation.
        J Neurosci. 1995; 15: 3886-3895
        • Kobayashi J.
        • Mackinnon S.E.
        • Watanabe O.
        • et al.
        The effect of duration of muscle denervation on functional recovery in the rat model.
        Muscle Nerve. 1997; 20: 858-866
        • Raineteau J.
        • Schwab M.E.
        Plasticity of motor systems after incomplete spinal cord injury.
        Nat Rev Neurosci. 2001; 2: 263-273
        • Kramer J.L.
        • Lammertse D.P.
        • Schubert M.
        • Curt A.
        • Steeves J.D.
        Relationship between motor recovery and independence after sensorimotor-complete cervical spinal cord injury.
        Neurorehabil Neural Repair. 2012; 26: 1064-1071
        • Steeves J.
        • Lammertse D.
        • Kramer J.
        • et al.
        Outcome measures for acute/subacute cervical sensorimotor complete (AIS-A) spinal cord injury during a phase 2 clinical trial.
        Top Spinal Cord Inj Rehabil. 2012; 18: 1-14
        • Dietz V.
        • Curt A.
        Neurological aspects of spinal-cord repair: promises and challenges.
        Lancet Neurol. 2006; 5: 688-694
        • Kirshblum S.
        • Botticello A.
        • Lammertse D.P.
        • Marino R.J.
        • Chiodo A.E.
        • Jha A.
        The impact of sacral sensory sparing in motor complete spinal cord injury.
        Arch Phys Med Rehabil. 2011; 92: 376-383
        • Denis A.R.
        • Feldman D.
        • Thompson C.
        • Mac-Thiong J.M.
        Prediction of functional recovery six months following traumatic spinal cord injury during acute care hospitalization.
        J Spinal Cord Med. 2018; 41: 309-317
        • Kirshblum S.
        Rehabilitation of spinal cord injury.
        in: Frontera W.R. DeLisa J.A. Gans B.M. Robinson L.R. Bockeneck W. Chase J. DeLisa’s Physical Medicine and Rehabilitation, Principles and Practice. Lippincott Williams & Wilkins, Philadelphia2005: 1715-1752
        • Jug M.
        • Kejžar N.
        • Vesel M.
        • et al.
        Neurological recovery after traumatic cervical spinal cord injury is superior if surgical decompression and instrumented fusion are performed within 8 hours versus 8 to 24 hours after injury: a single center experience.
        J Neurotrauma. 2015; 32: 1385-1392
        • Grassner L.
        • Wutte C.
        • Klein B.
        • et al.
        Early decompression (< 8 h) after traumatic cervical spinal cord injury improves functional outcome as assessed by spinal cord independence measure after one year.
        J Neurotrauma. 2016; 33: 1658-1666
        • Furlan J.C.
        • Fehlings M.G.
        The impact of age on mortality, impairment, and disability among adults with acute traumatic spinal cord injury.
        J Neurotrauma. 2009; 26: 1707-1717
        • Wilson J.R.
        • Grossman R.G.
        • Frankowski R.F.
        • et al.
        A clinical prediction model for long-term functional outcome after traumatic spinal cord injury based on acute clinical and imaging factors.
        J Neurotrauma. 2012; 29: 2263-2271
        • Wilson J.R.
        • Davis A.M.
        • Kulkarni A.V.
        • et al.
        Defining age-related differences in outcome after traumatic spinal cord injury: analysis of a combined, multicenter dataset.
        Spine J. 2014; 14: 1192-1198
        • Cifu D.X.
        • Seel R.T.
        • Kreutzer J.S.
        • Marwitz J.
        • McKinley W.O.
        • Wisor D.
        Age, outcome and rehabilitation costs after tetraplegia spinal cord injury.
        NeuroRehabilitation. 1999; 12: 177-185
        • Scivoletto G.
        • Morganti B.
        • Molinari M.
        Neurologic recovery of spinal cord injury patients in Italy.
        Arch Phys Med Rehabil. 2004; 85: 485-489
        • Jakob W.
        • Wirz M.
        • van Hedel H.J.
        • Dietz V.
        Difficulty of elderly SCI subjects to translate motor recovery—’’body function’’—into daily living activities.
        J Neurotrauma. 2009; 26: 2037-2044
        • Petland W.
        • McColl M.A.
        • Rosenthal C.
        The effect of aging and duration of disability on long term health outcomes following spinal cord injury.
        Paraplegia. 1995; 33: 367-373
        • Osterthun R.
        • Tjalma T.A.
        • Spijkerman D.C.M.
        • et al.
        Functional independence of persons with long-standing motor complete spinal cord injury in the Netherlands.
        J Spinal Cord Med. 2020; 43: 380-387
        • Nott M.T.
        • Baguley I.J.
        • Heriseanu R.
        • et al.
        Effects of concomitant spinal cord injury and brain injury on medical and functional outcomes and community participation.
        Top Spinal Cord Inj Rehabil. 2014; 20: 225-235
        • Schönherr M.C.
        • Groothoff J.W.
        • Mulder G.A.
        • Eisma W.H.
        Prediction of functional outcome after spinal cord injury: a task for the rehabilitation team and the patient.
        Spinal Cord. 2000; 38: 185-191
        • Curt A.
        • Schwab M.E.
        • Dietz V.
        Providing the clinical basis for new interventional therapies: refined diagnosis and assessment of recovery after spinal cord injury.
        Spinal Cord. 2004; 42: 1-6
        • Kirshblum S.
        • Waring III, W.
        Updates for the International Standards for Neurological Classification of Spinal Cord Injury.
        Phys Med Rehabil Clin N Am. 2014; 25: 505-517
        • Marino R.J.
        • Barros T.
        • Biering-Sorensen F.
        • et al.
        International standards for neurological classification of spinal cord injury.
        J Spinal Cord Med. 2003; 26: S50-S56
        • Catz A.
        • Itzkovich M.
        • Agranov E.
        • Ring H.
        • Tamir A.
        SCIM—spinal cord independence measure: a new disability scale for patients with spinal cord lesions.
        Spinal Cord. 1997; 35: 850-856
        • Anderson K.D.
        • Acuff M.E.
        • Arp B.G.
        • et al.
        United States (US) multi-center study to assess the validity and reliability of the Spinal Cord Independence Measure (SCIM III).
        Spinal Cord. 2011; 49: 880-885
        • Itzkovich M.
        • Gelernter I.
        • Biering-Sorensen F.
        • et al.
        The Spinal Cord Independence Measure (SCIM) version III: reliability and validity in a multi-center international study.
        Disabil Rehabil. 2007; 29: 1926-1933
        • Fox I.
        • Hoben G.
        • Komaie G.
        • et al.
        Nerve transfer surgery in cervical spinal cord injury: a qualitative study exploring surgical and caregiver participant experiences [published online ahead of print September 27, 2019]. Disabil Rehabil.
        • Krishna V.
        • Andrews H.
        • Varma A.
        • Mintzer J.
        • Kindy M.
        • Guest J.
        Spinal cord injury: how can we improve the classification and quantification of its severity and prognosis?.
        J Neurotrauma. 2014; 31: 215-227
        • Aidinoff E.
        • Front L.
        • Itzkovich M.
        • et al.
        Expected spinal cord independence measure, third version, scores for various neurological levels after complete spinal cord lesions.
        Spinal Cord. 2011; 49: 893-896
        • Rudhe C.
        • van Hedel H.J.
        Upper extremity function in persons with tetraplegia: relationships between strength, capacity, and the spinal cord independence measure.
        Neurorehabil Neural Repair. 2009; 23: 413-421
        • Kirshblum S.C.
        • Bloomgarden J.
        • Nead C.
        • McClure I.
        • Forrest G.
        • Mitchell J.
        Rehabilitation of spinal cord injury.
        in: Kirshblum S.C. Campagnolo D. Spinal Cord Medicine. 2nd ed. Lippincott Williams & Wilkins, Philadelphia2011: 309-340
        • Kalsi-Ryan S.
        • Beaton D.
        • Curt A.
        • Popovic M.R.
        • Verrier M.C.
        • Fehlings M.G.
        Outcome of the upper limb in cervical spinal cord injury: profiles of recovery and insights for clinical studies.
        J Spinal Cord Med. 2014; 37: 503-510
        • Kaminski L.
        • Cordemans V.
        • Cernat E.
        • M’Bra K.I.
        • Mac-Thiong J.M.
        Functional outcome prediction after traumatic spinal cord injury based on acute clinical factors.
        J Neurotrauma. 2017; 34: 2027-2033
        • Hentz V.R.
        • LeClercq C.
        Surgical Rehabilitation of the Upper Limb in Tetraplegia.
        Saunders Ltd, Philadelphia2002
        • Curtin C.M.
        • Gater D.R.
        • Chung K.C.
        Upper extremity reconstruction in the tetraplegic population, a national epidemiologic study.
        J Hand Surg Am. 2005; 30: 94-99
        • Bertelli J.A.
        • Ghizoni M.F.
        Nerve transfers for elbow and finger extension reconstruction in midcervical spinal cord injuries.
        J Neurosurg. 2015; 122: 121-127
        • Cain S.A.
        • Gohritz A.
        • Fridén J.
        • van Zyl N.
        Review of upper extremity nerve transfer in cervical spinal cord injury.
        J Brachial Plex Peripher Nerve Inj. 2015; 10: e34-e42
        • Anderson K.D.
        • Fridén J.
        • Lieber R.L.
        Acceptable benefits and risks associated with surgically improving arm function in individuals living with cervical spinal cord injury.
        Spinal Cord. 2009; 47: 334-338
      2. Fox I, Dengler J, Curt A, et al. Degree of upper extremity function recovery in cervical spinal cord injury: implications for peripheral nerve transfer surgery to restore upper limb function. Paper presented at: 58th ISCoS Annual Scientific Meeting; November 5-7, 2019; France.

        • Kirshblum S.
        • Millis S.
        • McKinley W.
        • Tulsky D.
        Late neurologic recovery after traumatic spinal cord injury.
        Arch Phys Med Rehabil. 2004; 85: 1811-1817
        • Ditunno Jr., J.F.
        • Cohen M.E.
        • Hauck W.W.
        • Jackson A.B.
        • Sipski M.L.
        Recovery of upper-extremity strength in complete and incomplete tetraplegia: a multicenter study.
        Arch Phys Med Rehabil. 2000; 81: 389-393
        • Waters R.L.
        • Adkins R.H.
        • Yakura J.S.
        • Sie I.
        Motor and sensory recovery following complete tetraplegia.
        Arch Phys Med Rehabil. 1993; 74: 242-247
        • Waters R.L.
        • Adkins R.H.
        • Yakura J.S.
        • Sie I.
        Motor and sensory recovery following incomplete tetraplegia.
        Arch Phys Med Rehabil. 1994; 75: 306-311
        • Ditunno Jr., J.F.
        • Cohen M.E.
        • Hauck W.W.
        • Jackson A.B.
        • Sipski M.L.
        Recovery of upper-extremity strength in complete and incomplete tetraplegia: a multicenter study.
        Arch Phys Med Rehabil. 2000; 81: 389-393
        • Catz A.
        • Greenberg E.
        • Itzkovich M.
        • Bluvshtein V.
        • Ronen J.
        • Gelernter I.
        A new instrument for outcome assessment in rehabilitation medicine: spinal cord injury ability realization measurement index.
        Arch Phys Med Rehabil. 2004; 85: 399-404
        • Kalsi-Ryan S.
        • Beaton D.
        • Curt A.
        • et al.
        The Graded Redefined Assessment of Strength Sensibility and Prehension (GRASSP): reliability and validity.
        J Neurotrauma. 2012; 29: 905-914