Cervical nerve 5 palsy is a well-known complication following decompressive surgery for cervical spondylosis that presents with weakening of the C5 myotome, including the deltoid and biceps brachii muscles, by at least one Medical Research Council (MRC) grade.1 The supraspinatus and infraspinatus muscles are also part of the C5 myotome and can be affected as well. Unfortunately, occurrence of C5 palsy is relatively common, with an estimated incidence of 5%–14%.1–5 The prognosis of postoperative C5 palsy is generally favorable. However, a subset of patients do not recover useful strength and experience a lifelong decrease in their quality of life. The natural history of recovery is variable, with full recovery ranging from 41% to 91%6 and estimates as high as 17%7 of patients who do not experience neurological improvement.8,9
For patients who ultimately do not experience recovery of useful strength, treatment options have historically been limited to supportive care.7 Recently, however, there has been interest in the potential for nerve transfers to restore the function of the C5 myotome in patients with severe and nonimproving C5 palsy.8,10–12 Historically, nerve transfer surgeries have been offered as treatment for brachial plexus preganglionic avulsion injuries in which nerve grafting was not indicated; however, nerve transfer surgery has been applied successfully to an increasing number of indications, including postganglionic brachial plexus injury, spinal cord injury,13 and the focus of this study, idiopathic postoperative C5 palsy.7,10
One notable concern is that there is a temporal limitation for nerve transfer surgery for reconstruction of the C5 myotome. The nerve transfer must be completed, and the muscles reinnervated by axons, prior to the occurrence of muscle fibrosis associated with prolonged denervation.14 This phenomenon of muscle fibrosis is described as occurring 12–18 months after denervation.15
To determine which patients are candidates for nerve transfer, a better understanding of C5 palsy prognosis is needed. The primary purpose of this retrospective cohort study is to determine at which time point after surgery patients are less likely to recover and would therefore potentially benefit from referral for nerve transfer surgery. This would help providers and patients to weigh the benefits and risks of offering nerve transfer surgery for C5 myotome reconstruction during the window of opportunity of early denervation, prior to muscle atrophy and fibrosis at which point nerve transfers would not be viable.
Methods
After obtaining institutional review board approval, we conducted a retrospective chart review identifying 72 patients who developed delayed C5 palsy after undergoing decompressive cervical surgery involving the C4–5 segment at a single academic tertiary-care institution from January 2000 to January 2020. Patients initially had a postoperative examination without definite C5 palsy, followed by a delayed C5 palsy that occurred during their hospital course. Variables collected from the electronic medical record included age, biological sex, operations performed, anterior versus posterior approach, number of operated spinal segments, presence and degree of foraminal stenosis, history of diabetes or peripheral vascular disease, tobacco use, alcohol use, and MRC motor strength (graded from 0 to 5) of left and right shoulder abduction and elbow flexion. Patients with postoperative follow-up of less than 12 months were excluded. MRC grades were recorded at the following time points: preoperatively; immediately postoperatively; at discharge; and at 2 weeks, 3 months, 6 months, and 12 months postoperatively.
Useful recovery from C5 palsy was defined as an MRC grade of 3 or greater for both shoulder abduction and elbow flexion. Patients with MRC grade 2 or less in shoulder abduction and/or elbow flexion were considered to have nonuseful strength. This definition was used in accordance with clinical relevance.16,17 Severe C5 palsy was defined as MRC grade 2 or less strength in shoulder abduction and/or elbow flexion. Mild C5 palsy was defined as MRC grade 3 or 4 strength in shoulder abduction and/or elbow flexion.
Given the temporal nature of the data, discrete time survival analysis methodology was employed, with univariable robust logistic regression models used to identify independent demographic and clinical risk factors for recovery from severe C5 palsy. Consistent with variables identified from the literature,4,18–23 discrete time survival analysis using multivariable robust logistic regression models fitted by sex, number of operative levels, surgical approach, and degree of foraminal stenosis were used for analysis of factors related to recovery from severe C5 palsy. We omitted variables relevant to foraminotomy due to low sample representation and did not collect data on ossification. A Poisson regression model was used to determine the probability of recovery from severe C5 palsy at different time points postoperatively, along with associated 95% confidence intervals.
Statistical analysis was performed with Stata version 16.1 (StataCorp). Values of p were two-tailed with a significance level of 0.05.
Results
The mean patient age was 62.5 years, and 36.1% (n = 26) of patients were female. Of the total sample, 41.7% (n = 30) were categorized as having severe C5 palsy with weakness below MRC grade 3. Throughout the study period, 21 patients (70%) recovered to a useful strength of MRC grade 3 or greater, but 9 patients (30%) did not recover useful strength. Further summary statistics can be found in Table 1.
Characteristics of patients who experienced postoperative C5 palsy
| Value | |
|---|---|
| No. of patients | 72 |
| Mean age, yrs | 62.5 |
| Female sex | 26 (36.1) |
| Diabetes history | 20 (27.8) |
| Peripheral vascular disease history | 7 (9.7) |
| Current tobacco use | 8 (11.1) |
| History of tobacco use | 39 (54.2) |
| Current alcohol use | 40 (55.6) |
| Anterior approach | 11 (15.3) |
| Posterior approach | 61 (84.7) |
| Mean no. of treated levels | 2.9 |
| Foraminotomy at C4–5 | 12 (16.7) |
Values are presented as the number of patients (%) unless stated otherwise.
Differences between patients who experienced mild C5 palsy compared with severe C5 palsy are detailed in Table 2. Forty-three percent of patients with severe C5 palsy had a history of diabetes, compared with 16.7% of those with mild C5 palsy (p = 0.01).
Comparison of patient factors, comorbidities, and surgical factors between mild and severe C5 palsy groups
| Mild C5 Palsy | Severe C5 Palsy | p Value | |
|---|---|---|---|
| No. of patients | 42 | 30 | |
| Mean age, yrs | 60.7 | 64.3 | 0.44 |
| Female sex | 16 (38.1) | 10 (33.3) | 0.68 |
| Diabetes history | 7 (16.7) | 13 (43.3) | 0.01 |
| Peripheral vascular disease history | 5 (11.9) | 2 (6.7) | 0.46 |
| Current tobacco use | 4 (9.5) | 4 (13.3) | 0.61 |
| History of tobacco use | 22 (52.4) | 17 (56.7) | 0.72 |
| Current alcohol use | 24 (57.1) | 16 (53.3) | 0.75 |
| Anterior approach | 7 (16.7) | 4 (13.3) | 0.70 |
| Posterior approach | 35 (83.3) | 26 (86.7) | 0.70 |
| Mean no. of treated levels | 2.6 | 3.1 | 0.09 |
| Foraminotomy at C4–5 | 7 (16.7) | 5 (16.7) | 0.94 |
Values are presented as the number of patients (%) unless stated otherwise.
Delayed postoperative imaging after occurrence of C5 palsy, either MRI or CT, was performed in 53 patients (73.6%). These studies did not demonstrate evidence of hardware complication or other iatrogenic complication.
At 3 months postoperatively in the severe C5 palsy group, 12 patients (40%) recovered useful strength. At 6 months postoperatively, 18 patients (60%) recovered useful strength. At 12 months postoperatively, 21 patients (70%) recovered useful strength (Fig. 1).
Flowchart demonstrating the degree of persistent severe postoperative C5 palsy at different time points.
Of the 12 patients with persistent severe weakness (MRC grades 0–2) at 6 months postoperatively, 3 patients (25%) recovered to useful strength at 12 months postoperatively, and 9 patients (75%) had persistent MRC grade of 2 or less. Further subanalysis of this group at 6 months showed that 8 patients had MRC grade 2 strength, and 4 patients had MRC grade 0 or 1. Of these 8 patients with MRC grade 2, 3 patients (37.5%) recovered to useful strength at the 12-month postoperative time point. No patient with MRC grade 0 or 1 strength at 6 months postoperatively recovered to useful strength at the 12-month time point.
On univariate logistic regression analysis to determine clinical prognostic factors for recovery of useful strength for patients with severe C5 palsy, no statistically significant risk factors were found across demographic, procedural, or weakness characteristics observed for both patient cohorts of interest (Table 3).
Univariate and multivariate analyses of patients with severe C5 palsy to assess for significant patient factors with recovery of useful strength
| OR | 95% CI | p Value | |
|---|---|---|---|
| Univariate analysis | |||
| Age | 1.01 | 0.98–1.03 | 0.67 |
| Female sex | 1.96 | 0.76–5.06 | 0.17 |
| Posterior approach | 1.63 | 0.35–7.59 | 0.54 |
| >3 levels | 1.32 | 0.48–3.66 | 0.59 |
| Severe foraminal stenosis | 1.50 | 0.28–7.90 | 0.63 |
| Foraminotomy | 0.82 | 0.25–2.69 | 0.74 |
| Foraminal stenosis | 1.53 | 0.33–7.16 | 0.59 |
| Diabetes | 1.02 | 0.40–2.60 | 0.96 |
| Peripheral vascular disease | 0.67 | 0.08–5.64 | 0.71 |
| Current smoker | 1.11 | 0.29–4.18 | 0.88 |
| Current alcohol use | 0.69 | 0.27–1.74 | 0.43 |
| Multivariate analysis | |||
| Female sex | 4.73 | 1.23–18.13 | 0.02 |
| Posterior approach | 1.31 | 0.23–7.42 | 0.76 |
| >3 levels | 1.67 | 0.44–6.27 | 0.45 |
| Severe foraminal stenosis | 0.97 | 0.12–7.88 | 0.98 |
For patients with severe C5 palsy, multivariate logistic regression of recovery fitted by sex, number of operative levels, surgical approach, and presence of severe foraminal stenosis was performed. Female sex was associated with recovery to useful strength, and this finding was statistically significant (OR 4.7, CI 1.23–18.13; p = 0.02) (Table 3).
Using a Poisson regression model, the probability of recovery at different time points was calculated. At 2 weeks postoperatively, patients with persistent severe C5 palsy had a 70% probability of recovering useful strength. At 3 months postoperatively, patients with severe C5 palsy had a 50% probability of recovering useful strength. At 6 months postoperatively, patients with severe C5 palsy had a 25% chance of recovering useful strength (Fig. 2).
Graph demonstrating different time points following severe postoperative C5 palsy, and the probability of a patient recovering to useful strength by 1 year. Error bars indicate 95% CIs.
Discussion
Incidence and Natural History of C5 Palsy
The pathophysiology of postoperative C5 palsy remains unclear. Various mechanisms of injury have been investigated, including direct nerve root injury during surgery, nerve root ischemia, postdecompression nerve root tethering, and reperfusion injury following decompression.18,24–26 The etiology may certainly be multifactorial.4
Bydon et al.20 reviewed 1001 operations involving the C4–5 level in the setting of degenerative cervical spine disease; the overall C5 palsy rate was 5.2%. The rate with an anterior approach was 1.6%, and the rate with a posterior approach was 8.6%. The risk of C5 palsy increased with the performance of foraminotomy (both anterior and posterior) and with the addition of corpectomy. The rate of C5 palsy after posterior foraminotomy was reported to be 14.5%. Posterior surgical approach is a documented risk factor for development of postoperative C5 palsy.20,27 Other identified risk factors include a higher degree of anterior compression, age, stenosis of the C4–5 vertebral foramen, male sex, performance of laminectomy, and ossification of the posterior longitudinal ligament.4,18,21,23
Prognosis of postoperative C5 palsy is favorable, with full recovery (to preoperative strength or better) usually occurring between 3 and 8 months after onset and rates of full recovery ranging from 41% to 78%. In some cases, time to full recovery extended to 5 years postsurgery.4,7–9,28 Rates of partial recovery, defined as recovery of strength less than preoperative levels, range from 25% to 56%. Patients less frequently can experience no improvement in their symptoms, with reported rates as high as 10%. In our series, 38 patients (52.8%) experienced a full recovery, 25 patients (34.7%) experienced a partial recovery to antigravity strength or greater, and 9 patients (12.5%) did not recover useful strength at the 12-month follow-up.
Treatment Options for C5 Palsy
Existing treatment options for idiopathic postoperative C5 palsy are limited.7 There is little evidence that interventions other than supportive care offer any significant benefit.7 Treatments that have been attempted and studied include the use of steroids,18 foraminotomy at the C4–5 level on the affected side,29 and prophylactic foraminotomy at the time of the index operation.2 There is mixed evidence regarding the efficacy of these interventions, and presently, there is no standardized evidence-based treatment for C5 palsy.
An emerging treatment option of interest for C5 palsy is the use of nerve transfers to reconstruct the function of the affected C5 myotome. Historically, nerve transfers have been used to treat patients with nerve root avulsion injuries where nerve grafting would not be effective. These procedures involve using an intact nerve with duplicated function to restore function to an injured nerve.30,31 Patients with traumatic nerve injuries have exhibited enhanced strength recovery after treatment with nerve transfer techniques.32–34 Nerve transfer surgery is thought to be most beneficial when postoperative strength fails to recover to antigravity strength (MRC grade 3 or greater), which is considered to be useful motor function.16,17
Currently, nerve transfer procedures are showing promise in novel applications, including restoration of selected functions after spinal cord injury,35 sensory reinnervation,30 targeted muscle reinnervation to prevent pain postamputation,36 and improvement of bladder control.30,31 It is possible that nerve transfers may produce similarly favorable outcomes for postoperative C5 palsy patients given that nerve transfers can provide axon donors distal to the area of injury in postoperative C5 palsy. The most appropriate candidates for potential nerve transfer surgery following C5 palsy are patients who have not recovered useful strength in shoulder abduction and/or elbow flexion.
As a general principle for nerve transfers, there is a specified window of time during which nerve transfers have the potential to restore neurological function. Muscles that are denervated undergo a slow atrophy and decline, and muscles undergo irreversible cell death if they do not become neurotized (reconnected to axons). Once muscles reach late-stage denervation, it cannot be reversed by neurotization.37 Myocyte death has been reported to occur 18–24 months following denervation.38
Due to the time constraints presented by denervated muscle, optimal timing for nerve transfer surgery is generally regarded to be 3–9 months after injury. This is because it takes a period of several weeks to months for axons to grow from the site of nerve coaptation to the muscle motor end plate, given the expected growth rate of approximately 1 mm/day.37,39,40 This timing is recommended to allow time for axons to grow from the site of coaptation to the neuromuscular junctions, prior to myofibril death.
One of the most important challenges with determining whether to offer nerve transfer surgery to patients with persistent clinically significant C5 palsy is the optimal timing of intervention. The ability to predict which patients have a low chance of recovery from C5 palsy and are good candidates for nerve transfer surgery is necessary to minimize unnecessary interventions. The use of electrodiagnostic studies may also have some utility in prognosticating recovery.10 Prior literature regarding timing of recovery from C5 palsy reports that maximal recovery generally occurs within 6 months,7 although it can occur up to 2 years postoperatively.2 However, interpretation of prior research is limited by lack of standardization in defining recovery of useful strength.
There is a paucity of data regarding outcomes of nerve transfer surgery for the reconstruction of the C5 myotome after postoperative C5 palsy.7,10 However, there is a large amount of data for the efficacy of reconstruction of the C5 and C6 myotomes after upper trunk injury in the brachial plexus.41–43 For complete upper-trunk brachial plexus injuries in adults, nerve transfers have been reported to achieve an average shoulder abduction of 92°, with most patients recovering at least MRC grade 3 strength in shoulder abduction and the majority of patients recovering at least MRC grade 4 in elbow flexion.44–46 Nerve transfer surgery therefore represents a viable therapeutic option for patients with failure to improve to useful strength after postoperative C5 palsy.
In our study population, 30 patients had severe postoperative C5 palsy. At 12 months postoperatively, 21 patients (70%) recovered useful strength, and 9 patients (30%) had persistent severe C5 palsy without recovery of useful strength. At 3 months postoperatively, patients had a 50% chance of recovering useful strength. At 6 months postoperatively, patients had a 25% chance of recovering useful strength.
Our data suggest that for patients with severe persistent C5 palsy at 3 months postoperatively, given the low probability of recovery of useful strength, referral to a quaternary care center with a complex peripheral nerve program would be reasonable to establish care. Although referral at 3 months postoperatively will result in referrals that are nonoperative given that some patients will recover at 6 months, this early referral will allow sufficient time for serial examinations, electrodiagnostic testing, and assessing candidacy for nerve transfer surgery for C5 myotome reconstruction if the patient does not recover useful strength with close follow-up.
There are several limitations to this study. The small sample size of our study may limit generalizability. Retrospective data collection may also have resulted in sampling bias.
Conclusions
The majority of patients with severe C5 palsy recover useful strength in their C5 myotome within 12 months of onset. However, at 3 months postoperatively, patients with persistent severe C5 palsy had only a 50% chance of recovering useful strength after 12 months. Lack of recovery of useful strength at 3 months postoperatively is a reasonable time point for referral to a complex peripheral nerve center to establish care for serial examinations and electrodiagnostic studies and to determine candidacy for nerve transfer surgery if severe C5 palsy persists.
Acknowledgments
We thank James Henderson at the University of Michigan’s Consulting for Statistics, Computing, and Analytics Research (CSCAR) center for helpful analytical guidance.
Disclosures
Dr. Park: consultant for Globus, NuVasive, Accelus, and DePuy Synthes; royalties from Globus; and non–study-related funding from SI Bone, DePuy Synthes, the International Spine Study Group, and Cerapedics.
Author Contributions
Conception and design: Park, Saadeh. Acquisition of data: Saadeh, Chopra, Olsen. Analysis and interpretation of data: Saadeh, Chopra, Kashlan. Drafting the article: Saadeh, Chopra. Critically revising the article: Park, Saadeh, Chopra, Smith, Kashlan, Yang. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Park. Statistical analysis: Chopra, Kashlan. Administrative/technical/material support: Park, Saadeh. Study supervision: Park, Saadeh.
Supplemental Information
Previous Presentations
This work was presented in abstract form at Spine Summit 2022—38th Annual Meeting of the Section on Disorders of the Spine and Peripheral Nerves, Las Vegas, Nevada, February 24, 2022, and won the Charles Kuntz Scholar Award.
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