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J Neurosurg Spine 2023 39 355
J Neurosurg Spine 2023 39 355
OBJECTIVE High cervical spinal cord injury (SCI) results in complete loss of upper-limb function, resulting in debili-
tating tetraplegia and permanent disability. Spontaneous motor recovery occurs to varying degrees in some patients,
particularly in the 1st year postinjury. However, the impact of this upper-limb motor recovery on long-term functional out-
comes remains unknown. The objective of this study was to characterize the impact of upper-limb motor recovery on the
degree of long-term functional outcomes in order to inform priorities for research interventions that restore upper-limb
function in patients with high cervical SCI.
METHODS A prospective cohort of high cervical SCI (C1–4) patients with American Spinal Injury Association Impair-
ment Scale (AIS) grade A–D injury and enrolled in the Spinal Cord Injury Model Systems Database was included.
Baseline neurological examinations and functional independence measures (FIMs) in feeding, bladder management, and
transfers (bed/wheelchair/chair) were evaluated. Independence was defined as score ≥ 4 in each of the FIM domains
at 1-year follow-up. At 1-year follow-up, functional independence was compared among patients who gained recovery
(motor grade ≥ 3) in elbow flexors (C5), wrist extensors (C6), elbow extensors (C7), and finger flexors (C8). Multivariable
logistic regression evaluated the impact of motor recovery on functional independence in feeding, bladder management,
and transfers.
RESULTS Between 1992 and 2016, 405 high cervical SCI patients were included. At baseline, 97% of patients had
impaired upper-limb function with total dependence in eating, bladder management, and transfers. At 1 year of follow-up,
the largest proportion of patients who gained independence in eating, bladder management, and transfers had recovery
in finger flexion (C8) and wrist extension (C6). Elbow flexion (C5) recovery had the lowest translation to functional inde-
pendence. Patients who achieved elbow extension (C7) were able to transfer independently. On multivariable analysis,
patients who gained elbow extension (C7) and finger flexion (C8) were 11 times more likely to gain functional indepen-
dence (OR 11, 95% CI 2.8–47, p < 0.001) and patients who gained wrist extension (C6) were 7 times more likely to gain
ABBREVIATIONS ADL = activity of daily living; AIS = American Spinal Injury Association Impairment Scale; FIM = functional independence measure; ICSHT = International
Classification for Surgery of the Hand in Tetraplegia; MRC = Medical Research Council; SCI = spinal cord injury; SCIMS = Spinal Cord Injury Model Systems.
SUBMITTED January 21, 2023. ACCEPTED April 11, 2023.
INCLUDE WHEN CITING Published online May 26, 2023; DOI: 10.3171/2023.4.SPINE2382.
©AANS 2023, except where prohibited by US copyright law J Neurosurg Spine Volume 39 • September 2023 355
functional independence (OR 7.1, 95% CI 1.2–56, p = 0.04). Older age (≥ 60 years) and motor complete SCI (AIS grade
A–B) reduced the likelihood of gaining independence.
CONCLUSIONS After high cervical SCI, patients who gained elbow extension (C7) and finger flexion (C8) had signifi-
cantly greater independence in feeding, bladder management, and transfers than those with recovery in elbow flexion
(C5) and wrist extension (C6). Recovery of elbow extension (C7) also increased the capability for independent transfers.
This information can be used to set patient expectations and prioritize interventions that restore these upper-limb func-
tions in patients with high cervical SCI.
https://thejns.org/doi/abs/10.3171/2023.4.SPINE2382
KEYWORDS nerve transfer; spinal cord injury; functional recovery; upper-limb function; high tetraplegia; neurological
recovery; cervical
S
pinal cord injury (SCI) is a devastating condition, Spinal Injury Association Impairment Scale (AIS) grade
representing a significant public health problem. The A–D. We excluded patients with AIS grade E SCI, as well
incidence of SCI is estimated to be approximately as those with paraplegia, incomplete baseline or 1-year
54 cases per 1 million persons annually in the United follow-up neurological examinations, and missing func-
States, with 296,000 adults living with this condition.1,2 tional independence measures (FIMs).
Approximately 27% of SCIs are high cervical (C4 and
above), resulting in debilitating tetraplegia.1,3,4 This pre- Neurological Variables
dominantly affects young males in the prime years of their This study aimed to evaluate the association of motor
life.2 Regaining even partial arm and/or hand control can recovery in the upper limb with functional independence
significantly improve the patient’s quality of life.5,6 to perform relevant ADLs. Extracted data included dem-
Functional restoration after SCI has relied on maximiz- ographic variables, traumatic etiology, AIS grade, neuro-
ing the function that can be achieved by the muscles that logical level of injury, right and left motor levels, right and
remain under volitional control above the level of SCI.7 left sensory levels, and manual muscle testing results of
Upper-limb function may also substitute for other lost the key upper-extremity muscles at the time of rehabilita-
functions (e.g., wheelchair propulsion to compensate for tion and 1 year. All neurological examinations were per-
loss of ambulation).8 However, persons with high tetraple- formed according to the International Standards for Neu-
gia (i.e., C1–4 level) have no suitable residual volitional rological Classification of Spinal Cord Injury.16
motor function that can be utilized by current reconstruc-
tive and rehabilitative therapies (e.g., tendon transfers, Motor Levels
assistive arm, or hand therapies).9 Recent innovations in We defined the motor level as the lowest key muscle
reinnervation strategies utilizing nerve transfers have with Medical Research Council (MRC) grade ≥ 3/5 on
shown promise in restoring paralyzed upper-limb func- manual muscle testing, with all muscles rostral to this
tion in patients with high tetraplegia.10–12 The reanimation level intact (i.e., MRC grade ≥ 4/5). All muscles caudal
of upper-limb function in certain myotomes may translate to the SCI were required to have MRC grade ≤ 2/5. For
to functional independence in a range of activities.13 How-
the myotomes with no clinically testable muscles (i.e., C4
ever, to what degree nerve reanimation restores functional
and above), the most caudal dermatome with normal sen-
independence in activities of daily living (ADLs) remains
sory examination was the assumed motor level.17 Based
unknown.
on these criteria, the C1–4 motor levels were defined as
The objective of this study was to evaluate improve-
having normal sensation (light touch and pinprick), which
ments in function associated with recovery of each myo-
assumed normal motor function at the corresponding lev-
tome from C5 to C8 after a high cervical SCI. The goal
el. To address possible left/right asymmetry in the motor
was to guide patient counseling regarding expected func-
examinations, single motor level was defined on the basis
tional outcomes and to prioritize research in upper-limb
of only the best motor test result from the right and left
reanimation therapies for high cervical SCI.
sides.18
For SCI severity, AIS grades were defined as motor
Methods complete (AIS grade A–B) and motor incomplete (AIS
Study Design and Participants grade C–D). SCI was defined as symmetrical if the right
This study included a longitudinal cohort of SCI pa- and left motor levels were the same, or as asymmetrical
tients enrolled in the Spinal Cord Injury Model Systems if there was a difference of one or more levels.18,19 Motor
(SCIMS) database.14 This database contains prospectively recovery at 1-year follow-up was defined as MRC grade
collected data on SCI patients treated at one of the SCIMS ≥ 3/5 in a muscle that was MRC grade ≤ 2/5 at baseline.20
centers in the United States. A detailed description of the The included key upper-limb muscles were the elbow flex-
SCIMS database is available elsewhere.15 This study was ors (C5), wrist extensors (C6), elbow extensors (C7), and
approved by the institutional review board at Washington finger flexors (C8).
University.
We included adult (≥ 15 years of age) cervical SCI pa- Functional Outcomes
tients admitted to one of the SCIMS centers from 1992 The primary outcomes were independence in major
to 2016 with motor level of injury at C1–4 and American ADLs, as assessed in terms of FIMs at 1 year after SCI.21
TABLE 1. Clinical characteristics of the patients with high Yet, this group had the greatest proportion of patients who
cervical SCI (n = 405) stayed fully dependent in performing functions (eTable
Characteristic No. (%) of Patients 3). From baseline to 1-year follow-up, only 8% of patients
improved from motor complete to motor incomplete SCI
Age, yrs (Fig. 4). When stratified on the basis of complete and in-
<60 337 (83) complete injuries, the degree of motor recovery and re-
≥60 68 (17) sulting functional independence gained were greater in
Sex patients with incomplete injuries (eFig. 1A–C).
Male 344 (85)
Impact of Upper-Limb Motor Recovery on Overall
Female 61 (15)
Functional Independence
Traumatic etiology
At 1-year follow up, 20% of patients achieved the com-
Motor vehicle 175 (43) posite outcome of functional independence in eating,
Assault 53 (13) bladder management, and transfers. After 1 year of follow-
Sports injury 51 (13) up, combined recovery in the distal myotomes, including
Fall 116 (28) those for elbow extension (C7) and finger flexion (C8),
Other 4 (1) was significantly associated with increased functional in-
dependence as compared with recovery in the proximal
Iatrogenic 6 (1)
myotome, i.e., that for wrist extension (C6). Detailed re-
Injury to spinal column* sults of the comparison between recovery of the proximal
Traumatic SCI 275 (82) myotome versus that of the distal myotomes are given in
Nontraumatic SCI 59 (18) eTable 4. On multivariable analysis, after adjustment for
Spinal surgery† known variables that influence functional independence,
Surgery 324 (82) combined recovery of elbow extension (C7) and finger
flexion (C8) was significantly associated with higher odds
No surgery 73 (18)
of functional independence (OR 11, 95% CI 2.8–47, p <
Motor level‡ 0.001) as compared with recovery in wrist extension (C6)
C1 21 (5) (OR 7.1, 95% CI 1.2–56, p = 0.04) (Table 2). Age ≥ 60
C2 54 (13) years and motor complete SCI had a trend toward reduced
C3 76 (19) odds of gaining independence. The results of the multi-
C4 254 (63) variable regression are given in Table 2.
Severity of SCI, AIS grade
Sensitivity Analysis of the Influence of Potential
A 222 (55)
Confounding Factors
B 48 (12)
Better performing dominant upper-limb myotomes had
C 120 (29) no significant impact (all myotomes p > 0.05) on function-
D 12 (3) al outcomes at 1-year follow-up (eTable 5). Nontraumatic
Symmetry of SCI§ SCI was significantly associated with improved functional
Symmetrical 345 (85) outcomes as compared with traumatic SCI. Spinal surgery
Asymmetrical 60 (15) at the time of SCI trended toward improved functional
outcomes; however, this finding was statistically nonsig-
* Injury to the spinal column was defined as any vertebral injury, including nificant (eTable 6). The inclusion of both variables in the
fracture or dislocation from the occiput to coccyx. multivariable regression model did not add any prognostic
† Spinal surgery was defined as any decompression, reduction, and/or fusion
surgery performed at the time of SCI.
value (both p > 0.05). Upper-limb function was signifi-
‡ Motor level was defined as normal findings on sensory examinations at the cantly associated with increased independence in bladder
C1–4 level with all C5–T1 myotomes MRC grade ≤ 2. The best motor level management among those patients who used alternative
between the right and left sides was included. means to empty their bladder (i.e., indwelling catheter,
§ SCI was defined as symmetrical if the same motor levels were noted on intermittent catheterization, and/or surgical conduit) and
the right and left sides, or as asymmetrical if ≥ 1-level difference was noted was comparable to that of the patients with normal mictu-
between the right and left sides. rition (eTable 7).
Discussion
ered finger flexion (C8): 60% had independence in eating, There remains a lack of knowledge about the relation-
63% in bladder management, and 67% in transfers (Fig. ship between specific upper-limb motor functions and
3). Among those who recovered elbow extension (C7), a ADLs after high cervical SCI.26 Although prior studies
large proportion of patients (60%) gained independence have attempted to model recovery trajectories after cer-
in transfers. Among those who recovered wrist extension vical SCI, evidence evaluating the impact of upper-limb
(C6), 52% were independent in eating and 55% were inde- recovery in specific myotomes with functional indepen-
pendent in bladder management. The largest proportion dence remains limited.20,27–29 This important evidence gap
of patients (52%) had recovery in C5 level (elbow flexion). actively impairs clinical decision-making regarding op-
FIG. 2. Baseline and 1-year FIMs of eating (A), bladder management (B), and transfers (C) by motor levels in patients with high
cervical SCI (C1–4). Figure is available in color online only.
timal treatment strategies and patient counseling after a distal upper-limb function.9 The detailed ICSHT with po-
high cervical SCI. tential reconstructive options is given in eTable 8. Among
In this study, we addressed this gap by utilizing a pro- patients with cervical SCI, those with low tetraplegia (C5–
spective cohort of high cervical SCI patients to analyze 8 level) may have some residual motor capability, such as
the impact of upper-limb motor recovery on functional in- those patients classified in ICSHT groups 3–4.23 These
dependence in ADLs. Our goal with this analysis was 1) to patients usually have intact function up to wrist extension
inform patient counseling regarding functional recovery and forearm pronation that can be utilized by traditional
in patients with high cervical SCI and 2) to inform future reconstructive (tendon transfers) and reinnervation (nerve
research investment on interventions targeting upper-limb transfers) therapies to restore grasp, release, and elbow
motor reanimation (i.e., nerve transfer surgery) that may extension.12,32,33 In contrast, patients with high tetraplegia
yield the most benefits in functional outcomes. (C1–4 level) are completely paralyzed below the neck and
Our analysis demonstrated that high tetraplegic patients have no residual upper-extremity motor function (ICSHT
who recover elbow extension and finger flexion function group 0) (eTable 8). In these patients with high tetraple-
can gain independence in a range of ADLs. In addition, gia, targeted treatments used to protect the flaccid upper
elbow extension recovery resulted in increased indepen- limbs against contractures consist of splinting, orthosis,
dence in transfer capabilities. Consistent with established and range-of-motion exercises.7,31 Despite the paralysis of
evidence that incomplete SCI has substantial recovery po- the upper limbs in ICSHT group 0, healthy motor neuron
tential,20,28,30 incomplete injury was associated with higher pools exist within the spinal cord years after injury.34 Par-
rates of functional improvement and independence in ticularly, upper-limb muscles distal to the SCI maintain
ADLs compared with complete SCI. their connectivity with the lower motor neuron, permitting
Traditionally, no reconstructive therapies have been delayed nerve transfer surgery.35
available for high tetraplegic patients who do not recover Nerve transfer surgery is an innovative intervention
upper-limb motor function.3,26,31 The International Classi- that can harness the potential of nerve regeneration to
fication for Surgery of the Hand in Tetraplegia (ICSHT) is restore distal paralyzed target muscles.10,23,36 In the con-
a 10-group classification that indicates how preserved up- text of SCI, nerve transfers effectively bypass the injured
per-limb motor function can be utilized for reinnervation segment of the spinal cord, restoring meaningful function
and/or reconstructive surgical procedures to reanimate in the paralyzed muscles.35 Nerve transfers were only re-
FIG. 3. Recovery of upper-limb function at 1-year follow-up and its impact on the FIMs of eating (A), bladder management (B), and
transfers (C). At each level, MRC grade ≤ 2 represents no recovery, while MRC grade ≥ 3 represents recovery. Figure is available
in color online only.
and 1-year follow-up, we were unable to determine the 6. Anderson KD. Targeting recovery:priorities of the spinal
exact timing of expected recovery before 1 year. Future cord-injured population. J Neurotrauma. 2004;21(10):1371-
studies should focus on the trajectory of motor recovery 1383.
7. Kalsi-Ryan S, Verrier MC. A synthesis of best evidence for
and its correlation with functional independence. Second, the restoration of upper-extremity function in people with
1-year follow-up measures were available for only 59% tetraplegia. Physiother Can. 2011;63(4):474-489.
of patients. Although the characteristics of the included 8. Snoek GJ, IJzerman MJ, Hermens HJ, Maxwell D, Biering-
and excluded patients were similar, there may have been Sorensen F. Survey of the needs of patients with spinal cord
an unavoidable selection bias. Third, in the SCIMS data- injury:impact and priority for improvement in hand function
base, there was no documentation of reconstruction (i.e., in tetraplegics. Spinal Cord. 2004;42(9):526-532.
nerve or tendon transfer surgery) that could have improved 9. Bryden AM, Peljovich AE, Hoyen HA, Nemunaitis G, Kil-
gore KL, Keith MW. Surgical restoration of arm and hand
upper-limb function in certain myotomes. However, these function in people with tetraplegia. Top Spinal Cord Inj Re-
surgical procedures are underutilized, and only 0.4% of habil. 2012;18(1):43-49.
eligible tetraplegic patients undergo these procedures.44 10. Ray WZ, Chang J, Hawasli A, Wilson TJ, Yang L. Motor
In addition, a high cervical SCI (C1–4) has limited do- nerve transfers:a comprehensive review. Neurosurgery. 2016;
nor nerve or tendon options for transfer.23 Therefore, al- 78(1):1-26.
though nerve/tendon transfer surgery could be a potential 11. Khalifeh JM, Dibble CF, Van Voorhis A, et al. Nerve trans-
confounder, it should not interfere with our primary con- fers in the upper extremity following cervical spinal cord
clusions regarding how changes in neurological recovery injury. Part 2:Preliminary results of a prospective clinical
trial. J Neurosurg Spine. 2019;31(5):641-653.
impacted functional independence. Fourth, in the SCIMS 12. van Zyl N, Hill B, Cooper C, Hahn J, Galea MP. Expanding
database, only the functional independence measure was traditional tendon-based techniques with nerve transfers for
available. However, recent SCI studies have used the spi- the restoration of upper limb function in tetraplegia:a pro-
nal cord independence measure, which is a newer outcome spective case series. Lancet. 2019;394(10198):565-575.
metric.45 Future work should verify the reproducibility of 13. Nott MT, Baguley IJ, Heriseanu R, et al. Effects of concomi-
our findings using this alternative outcome.45 Finally, we tant spinal cord injury and brain injury on medical and func-
did not include an analysis of certain other characteristics tional outcomes and community participation. Top Spinal
Cord Inj Rehabil. 2014;20(3):225-235.
that could have impacted recovery, such as comorbid diag- 14. Chen Y, DeVivo MJ, Richards JS, SanAgustin TB. Spinal
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15. Ketchum JM, Cuthbert JP, Deutsch A, et al. Representative-
Our study demonstrated that, in patients with high tetra- ness of the Spinal Cord Injury Model Systems National Data-
plegia, recovery of elbow extension and finger flexion may base. Spinal Cord. 2018;56(2):126-132.
significantly enhance independence in major ADLs, such 16. Kirshblum S, Snider B, Rupp R, Read MS. Updates of the In-
as eating, bladder management, and transfers. The recovery ternational Standards for Neurologic Classification of Spinal
of elbow extension may substantially enhance the patient’s Cord Injury:2015 and 2019. Phys Med Rehabil Clin N Am.
2020;31(3):319-330.
transfer capability. These findings can be used to counsel 17. Schuld C, Franz S, Brüggemann K, et al. International stan-
patients about expected functional return and inform novel dards for neurological classification of spinal cord injury:
research innovation of interventions targeting restoration of impact of the revised worksheet (revision 02/13) on classifica-
upper-limb function in patients with high cervical SCI. tion performance. J Spinal Cord Med. 2016;39(5):504-512.
18. Javeed S, Greenberg JK, Zhang JK, et al. Derivation and vali-
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