Abstract
Keywords
Introduction
Brachial plexus (BP) injuries possesses significant disability, and their surgical management is intricate due to diverse treatment options and injury patterns (Limthongthang et al., 2013). Surgical neurolysis is a procedure aimed at liberating an injured nerve from scar tissue or neighboring structures, facilitating regeneration (Andrisevic et al., 2014; Millesi et al., 1993). This technique allows the nerve to adapt to mechanical stress by gliding against surrounding tissue (Clarke et al., 1997). Additionally, it may not be effective in cases of nerve avulsion or transection. However, a recent systematic review comparing motor outcomes of various surgical techniques for BP injuries demonstrated that neurolysis presented the highest proportion of motor recovery (85%) compared to other techniques, which showed recovery rates below 73% (Armas-Salazar et al., 2022a, 2022b). Conversely, a study by Morgan et al. (2020) evaluating 21 patients with distal BP injury who underwent surgical neurolysis and open fasciotomy observed an improvement in the motor component, and other studies have shown effectiveness in pain relief and sensory recovery (Armas-Salazar et al., 2022a, 2022b; Morgan et al., 2020). Although the study by Morgan R. et al. did not evaluate surgical neurolysis as an isolated technique, it provides valuable insights into its potential usefulness. The current perception of surgical neurolysis among peripheral nerve surgeons often regards it as a preparatory technique preceding other interventions (Midha & Grochmal, 2019). Nevertheless, Li et al. (2019) reported on one of the largest series related to the surgical management of BP injuries, suggesting that surgical neurolysis might be suitable for patients with preserved nerve continuity and conduction, presenting compressive neuropathy (Li et al., 2019). Nonetheless, the true usefulness of this technique remains uncertain, underscoring the importance of assessing its impact on motor recovery in patients with brachial plexus neuropathy (BPN). Therefore, the objective of this study is to evaluate the motor outcomes of patients managed with surgical neurolysis.
Materials and Methods
Case Series
A total of 18 patients received treatment for BPN at the Neurosurgery Service. The study included adult patients of both genders, aged 18 to 65, with BPN injury diagnosed through preoperative electromyography showing a neurogenic pattern with positive fibrillations, polyphasic units, and an increased firing rate (Rempel & Diao, 2004). The inclusion criteria comprised patients with a high level of compromise (proximal third of the upper extremity) and motor impairment (British Medical Research Council motor grading scale BMRC score less than 5).
Patients with avulsion, preganglionic injury, pre-cervical lesion, and nerve transection were excluded based on magnetic resonance imaging, electrodiagnosis studies, and intraoperative findings for all patients. Data extraction focused on demographic information (age, gender), etiology, anatomical location of the injury, affected side, interval injury-surgery, and average follow-up period.
Clinical evaluation involved collecting pre- and postoperative data on the motor component using BMRC (James, 2007). The muscle with the highest percentage of innervation was chosen for the analysis (Tsao, 2007). Statistical analysis included calculating significant differences between pre-operative and post-operative BMRC scores using the Wilcoxon signed-rank test, and effect size was assessed using Cohen's Δ, with adjustments for small sample sizes. Subgroup analysis was conducted based on etiology. Data analysis was performed using SPSS 25.0 for Windows software (SPSS, Inc., Chicago, IL), considering a p-value < 0.05 significant.
The study series consisted of 18 patients. Among them, males predominated, accounting for 61% of the total. The average age at the time of injury was 34.06 ± 13.01 years. The primary etiology of BPN was post-traumatic in 11 cases (61%), followed by outlet thoracic syndrome (OTS) (22%), tumor (11%), and radiotherapy (6%). The most commonly affected region was the upper trunk (33%), followed by complete root lesions (C5-T1) at 27.8%. The mean interval between injury and surgical intervention was 10 ± 4.89 months, and the average follow-up period was 41.94 ± 39.84 months. For a summary of the clinical characteristics of the included patients, refer to Table 1.
Clinical and Demographic Characteristics of the Patients Included.
BMRC: British Medical Research Council; VT: Vehicular trauma; IT: Industrial trauma; SI: Stab injury; E: Ependymoma; A: Astrocytoma; SD: Standard deviation; IQR: Interquartile range; SA: Shoulder abduction; EF: Elbow flection; WE: Wrist extension.
* It was evaluated by the most representative function, which accounts for the highest percentage of motor component involvement (Tsao, 2007). **The data were represented as mean and standard deviation despite being a non-parametric sample because in the literature they are usually represented in this manner.
Surgical Technique
A “V-shaped” incision in the supraclavicular fossa was performed, tracing along the posterior border of the sternocleidomastoid and the inferior border of the clavicle (Figure 1 A-B). Care was taken to lift the platysma while preserving the external jugular vein. The guiding point of the approach, the omohyoid muscle, was observed and gently displaced using a surgical rubber band. Next, a dissection of the anterior interscalene triangle aponeurosis was performed, taking care to protect the phrenic nerve. This allowed exposure of the upper (C5-C6), middle (C7), and lower trunks (C8-T1) of the BP (Figure 1 C). During the surgical procedure, all trunks of the BP were thoroughly explored, and no muscles were sectioned. The main focus of the surgery was external neurolysis and decompression. This involved releasing the fascia, muscle, tendon, and vascular structures that were compressing the nerve. Scar tissue around the nervous structures was carefully removed (Figure1 D). Additionally, external neurolysis was performed, which consisted of creating longitudinal cuts along the epineural area of the nerves. The extent of neurolysis was determined based on the observed compression sites during the surgery.
Surgical technique. A. Surgical approach performed in the supraclavicular fossa B. “V-shaped” incision along the posterior border of the sternocleidomastoid muscle and the lower border of the clavicle C. Exposure of the neuroma-in-continuity located in the upper trunk (1) and its branches; suprascapular nerve (1.a), posterior division (1.b), and the upper trunk division to the anterior division (1.c). D. (1) represents a preserved nerve structure, contrasting the structures highlighted with numbers (2) and (3), which indicate the contact zone (arrow) that was released after surgical neurolysis.
Emphasis was placed on precisely defining the region and extent of plexus neurolysis. Initial determination relied on preoperative clinical assessment of muscles representing the predominant motor deficit, such as shoulder abduction (SA), elbow flexion (EF), and wrist extension (WE). Intraoperatively, specific neurolysis areas and extent were further refined based on observed nerve compression location and severity. The decision to proceed with isolated neurolysis hinged on several key considerations: the first one, the presence of a continuous injury; second, demonstration of compressive neuropathy via electrophysiological studies or imaging, and the last when feasible, intraoperative electrophysiological studies to confirm nerve conduction preservation.
Systematic Review
This was conducted following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines (McInnes et al., 2018). The primary objective was to determine the extent of motor status changes, as measured by the BMRC scale, after surgical neurolysis in adult patients with BPN. We included studies reporting pre- and post-operative motor clinical assessments of adult patients diagnosed with BPN who underwent primary surgical neurolysis. The review excluded pediatric populations with obstetric BP palsy, injuries located distally (arm, elbow, forearm, wrist, hand), case reports, basic science research, review articles, and publications in languages other than English. PubMed's advanced search was used with Mesh terms “Brachial Plexus Injury”, “Surgery”, “Humans” and “Adults”. This search yielded a total of 2298 articles published between 1968 and 2023, with no restrictions on study design, year of publication, or publication status. Figure 2 provides a summary of the selection criteria, search process, and data extraction. Motor outcomes were collected by obtaining preoperative and postoperative motor status data according to the BMRC scale from each study. The systematic review results were analyzed to determine the proportion of motor recovery reported in each study.
Flow diagram preferred reporting items for systematic review and meta-analysis (PRISMA) search strategy. BPN: Brachial Plexus Neuropathy.
Through a comprehensive bibliographic review, a total of 2298 articles published between 1968 and 2023 were initially identified. These articles underwent a screening process based on the review of titles and abstracts. Subsequently, 160 articles were selected in full-text format due to their relevance to BP surgery.
The most representative muscle was identified for each cervical root as follows: Deltoid (86%) for C5, Biceps (71%) for C6, Triceps (100%) for C7, and either first dorsal interosseous (100%) or Extensor indicis proprius (100%) for C8-T1. The percentage in parentheses indicates the extent of innervation received by the respective cervical root, and this information was derived from Tsao B.'s study in 2007. The muscle with the highest percentage of innervation was chosen for the analysis (Tsao, 2007).
Results
Case Series
The outcomes of the surgical intervention in the motor component are summarized in Table 2. In the long-term follow-up (mean 41.94 ± 39.84 months) after the surgical intervention, a significant increase of 58.52% in motor recovery, as assessed by BMRC, was observed compared to the preoperative status. The average preoperative BMRC score was 2.17 ± 1.15, which improved to 3.44 ± 1.34 postoperatively. These changes were found to be statistically significant (p = 0.003; d = 0.913), indicating a relevant motor recovery after the surgical intervention. Notably, there were no observed postoperative complications, and the surgery did not affect sensory function. Furthermore, a subgroup analysis based on the etiology of BPN (traumatic and non-traumatic - OTS, tumor, radiotherapy) was conducted. Regardless of the etiology, patients demonstrated significant motor improvement after the surgical intervention (p < 0.05) (Table 2). Regarding the location of the lesions, motor improvement was observed across all lesion patterns. The most substantial recovery was observed in C5-T1 injuries, with an improvement of 64.2%, followed by C7-C8-T1 (41.1%, C5-C6-C7 (39.9%), and C5-C6 (14.28%). Importantly, none of the patients experienced an isolated motor deficit or sensory impairment after surgery.
Clinical Outcomes After Surgical Neurolysis and Demographic Characteristics According to Etiology.
Data are shown as mean ± standard deviation or percentage.
Wilcoxon rank-sum test to compare the changes after the intervention.
Effect size calculated through Coheńs D with a correction factor for small sample sizes.
Increase (↑) or decrease (↓) relative to preoperative status.
BMRC: British medical research council motor grading scale.
*The group called non traumatic considers etiologies such as thoracic outlet syndrome, tumors, and post-radiotherapy lesions.
All patients in the series opted for surgery using neurolysis alone, as none of them exhibited signs of nerve transection during the intraoperative period (Figure 1C). Moreover, anatomical structures compressing the BP were identified in all cases (Figure 1D). Out of the 18 patients who underwent surgical management, 11 (61%) experienced improvement, 5 (28%) showed no change, and 2 (11%) exhibited a slight worsening after the intervention.
Systematic Review
A total of eight studies published between 1995 and 2020 were included in this analysis (Altaf et al., 2012; Dubuisson & Kline, 2002; Gousheh, 1995; Guang-Yao Li et al., 2019; Gutkowska et al., 2017; Kim et al., 2003; Morgan et al., 2020; Stewart & Birch, 2000), which are summarized in Table 3. These studies involved the evaluation of 240 patients regarding motor recovery outcomes. The most frequent study types were retrospective chart reviews and case series. However, no complete clinical trials (controlled, randomized, and blinded) were found in the included studies. Regarding the location of the lesions, they were found to be heterogeneous. Similarly, the delay in surgical management varied across studies, ranging from relatively early management between two weeks and four months (Altaf et al., 2012; Gousheh, 1995) to others that extended up to 10–11 months (Morgan et al., 2020). One significant limitation observed was the lack of clear reporting on the preoperative motor status in all studies published before 2019. However, postoperative motor status was reported in most studies, showing a proportion of motor recovery ≥ M3 in 75% of cases.
Summary of Articles Included in the Systematic Review of Motor Outcomes in Surgical Neurolysis for BPI.
Studies in which multiple techniques were; performed, among them the motor outcomes of surgical neurolysis were evaluated.
Mean (Standard deviation).
Median (Ranges). BMRC: British Medical Research Council; RCR: Retrospective chart review; CR: Consecutive recruitment; RCS: Retrospective case series; STI: Structured telephone interview; U: Unclear; NM: Not mentioned; SA: Shoulder abduction; EF: Elbow flection; WE: Wrist extension.
Discussion
Regarding motor outcomes in the case series, two patients (patient number 12 and 18) experienced worsening after the intervention. These patients shared similar clinical-demographic characteristics, being male patients in their third decade of life with right neuropathy due to a post-traumatic injury. Both underwent surgery 8 months after the injury, and their lesions were located in the upper trunks (C5-C6). However, upon analysis, none of these shared characteristics seem to correlate with the clinical worsening, as the group that demonstrated motor recovery also includes patients with similar clinical-demographic characteristics. Therefore, we hypothesize that the clinical worsening may be attributed to other factors, such as the impact of the nerve injury on muscle innervation (trophism) or deterioration resulting from neural/vascular insult during neurolysis (Gordon et al., 2011; Martin et al., 2018). Additionally, a possible considerable decrease in nerve conduction, indicated by a proximal compound motor action potential (cMAP) of more than 50% of the distal cMAP amplitude (<50% conduction) (Andrisevic et al., 2014), might have contributed to the outcome. Unfortunately, we were unable to conduct an electrophysiological study during surgery due to lack of available equipment for intraoperative analysis. Conducting such studies in the future could be relevant to determine an appropriate nerve conduction cut-off value in adults, enabling a better assessment of when it would be more suitable to perform a nerve graft instead of surgical neurolysis. Patients with similar characteristics could potentially benefit from nerve graft or nerve transfer procedures.
Evaluating the representative function of the affected nerves provides valuable insight into the patients’ improvement. However, we recognize that ideally, quantitative measures such as range of motion (ROM) would further enhance the precision of these assessments. Incorporating ROM measurements would allow for a more detailed analysis of the degree of functional recovery, providing not only an indication that improvement occurred but also a precise measure of the extent of that amelioration. Consequently, we propose that future studies should include ROM measurements as part of the motor evaluation to provide a more comprehensive understanding of the functional outcomes associated with neurolysis.
Furthermore, there exists a logical connection between surgical intervention using neurolysis and clinical recovery, as the patients who underwent surgical management presented with compressive neuropathy. This compressive neuropathy was observed in various etiologies, such as outlet thoracic syndrome (OTS), tumor presence, or the development of fibrosis secondary to trauma or radiotherapy.
In cases of OTS primarily involves compression of the brachial plexus between the first rib and the clavicle, often resulting in neurovascular compromise. The anatomical constraint leads to ischemic injury of the nerves, manifesting as pain, sensory deficits, and motor weakness in the affected upper limb (Dubuisson & Kline, 2002). Radiation therapy can induce fibrotic changes in the surrounding tissues of the brachial plexus, causing progressive constriction and compression of nerve fibers. Fibrosis restricts nerve mobility and disrupts microvascular circulation, contributing to chronic nerve hypoxia and subsequent motor dysfunction (Čebron et al., 2021; Warade et al., 2019). Tumors adjacent to or infiltrating the brachial plexus exert direct mechanical pressure on nerve roots or trunks, disrupting their normal function. Compression from tumors can lead to nerve entrapment, ischemia, and impaired nerve conduction, resulting in motor deficits and sensory abnormalities (Warade et al., 2019). Traumatic injuries to the brachial plexus, such as traction injuries, can cause immediate mechanical disruption of nerve fibers or lead to secondary fibrosis and scarring. The initial trauma disrupts nerve integrity, while subsequent inflammation and chronic phase following a fibrosis with further compromises nerve function by limiting their ability to conduct electrical signals and receive adequate blood supply (Dubuisson & Kline, 2002).
Regardless of the etiology, these conditions share a common pathophysiological mechanism (Čebron et al., 2021; Dubuisson & Kline, 2002; Warade et al., 2019) that involves nerve strangulation, leading to reduced blood flow and consequent motor impairment (Baxter et al., 2008). Surgical neurolysis effectively addresses it by releasing the compressed nervous structures through separation from the surrounding tissues. This phenomenon explains the observed improvement in patients, irrespective of the specific etiology, as all these conditions share the underlying pathophysiology associated with compressive neuropathy (as summarized in Table 3).
Regarding neurolysis, releasing compressing structures such as fascia, muscle, vessels, etc. is not considered neurolysis and is simply called decompression. In BP injuries, releasing scar tissue and inter fascicular lysis is performed which is called neurolysis. In these cases, the procedure was surgical neurolysis due to the decompression/external neurolysis performed in the non-traumatic cases, and the neurolysis carried out in the traumatic patients.
Limitations
Several factors must be considered when interpreting our findings. Firstly, the heterogeneity of follow-up periods, ranging from two to 156 months, may lead to variations in motor recovery estimates. Secondly, limitations in performing intraoperative electrophysiology in all cases may introduce biases in nerve integrity assessment. Additionally, the varied etiologies within our case series represent a potential source of variability in recovery rates, which may limit the generalizability of our findings. In our systematic review, limitations include the heterogeneity and quality of evidence, predominantly derived from studies with varying methodologies and levels of evidence. Moreover, some studies with higher evidence levels focused on pediatric populations, limiting direct applicability to adult patients (Andrisevic et al., 2014; Clarke et al., 1997). Additionally, our qualitative synthesis highlighted a scarcity of studies specifically evaluating neurolysis as a standalone technique (Morgan et al., 2020).
Upon analyzing the articles in Table 3, notable studies reported high motor recovery percentages with shorter lesion-surgery intervals. Giuffre et al. suggested an optimal surgical intervention window of up to six months post-injury, acknowledging the inflammatory scar tissue process between two and eight weeks post-injury that can complicate surgery (Giuffre et al., 2010; Hems, 2015; Noland et al., 2019). Current trends in peripheral nerve injury management favor complex techniques like nerve transfers and muscle/tendon transfers, underscoring the need for robust studies to clarify neurolysis role amidst these advancements.
Further Considerations
Our study aims to address gaps in current literature by proposing a well-designed, randomized trial evaluating neurolysis against other surgical alternatives. This prospective study will assess motor outcomes, range of motion, and quality of life across multiple time points, using rigorous methodologies to minimize bias and enhance study validity. We recognize that while neurolysis is often a preparatory step in multifaceted nerve repair strategies, our findings underscore its potential as an effective standalone technique for motor restoration in selected patient groups.
To address the current research gap, we propose a randomized trial comparing surgical neurolysis with alternative techniques like nerve grafting or transfer in brachial plexus injuries. With an effect size of d = 0.913 from our case series, we calculate needing 21 patients per group for 99% power. Assessments will use the BMRC scale, range of motion, and DASH questionnaire, alongside dynamometry and SF-36 for quality of life, preoperatively and at intervals up to 24 months post-surgery. Blinding will minimize bias, addressing demographics, injury severity, timing, and location comprehensively. This design aims to clarify neurolysis’ role, especially as a standalone treatment.
Clinical Considerations
The main objective of this study is not to establish surgical neurolysis as the superior technique or advocate its exclusive use over other surgical alternatives. We recognize that many surgeons view it as a preparatory procedure preceding other interventions such as nerve grafts or transfers, and it is not typically considered in isolation. Nevertheless, our analysis of the case series, combined with the existing literature, suggests that surgical neurolysis may offer valuable benefits for motor restoration in specific patient scenarios.
In light of these findings, we believe that surgical neurolysis should be regarded as an integral part of the surgical armamentarium, even as a standalone technique. While we acknowledge the need for more comprehensive evidence, the current results indicate its effectiveness in terms of motor recovery for patients with preserved nerve continuity and conduction, as well as those with compressive neuropathy.
Conclusions
Contrary to conventional assumptions, the findings of this case series and systematic review prompt us to reconsider the potential of surgical neurolysis for motor recovery in adult patients with BPN, particularly those presenting with continuous nerve injury and preserved nerve conduction associated with compressive neuropathic symptoms. Our study highlights promising outcomes that suggest surgical neurolysis may offer significant benefits in restoring motor function in these specific patient profiles. Nevertheless, given the absence of complete clinical trials, these results underscore the necessity to re-evaluate the utility of this technique through well-designed, adequately powered, randomized, and blinded clinical trials.
Footnotes
Ethics Statement
Prior to participation in this study, written informed consent was obtained from each patient. The study protocol and research procedures were reviewed and approved by the hospital's Research and Bioethics Committee under protocol number DI/16/403/03/152. All aspects of the study were conducted in compliance with the principles outlined in the Declaration of Helsinki and other relevant ethical guidelines to safeguard the rights, confidentiality, and well-being of the participants.
Funding
The authors received no financial support for the research, authorship, and/or publication of this article.
Declaration of Conflicting Interests
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Data Availability Statement
The data supporting the findings of this study are available on request from the corresponding author. The data are not publicly available due to privacy or ethical restrictions.