Original Article Retrospective Study of 57 Patients Submitted to Dorsal Root Entry Zone Lesioning by Radiofrequency for Brachial Plexus Avulsion Pain Marcio de Mendonça Cardoso1, Ricardo Gepp1, Henrique Caetano1, Ricardo Felipe1, Bernardo Martins2 BACKGROUND: Dorsal root entry zone (DREZ) lesioning may be used to treat neuropathic pain in patients with traumatic brachial plexus injuries. The clinical outcome after surgery is variable in the medical literature. We aimed to report the surgical outcome after DREZ lesioning by radiofrequency and to analyze prognostic factors such as the presence of a spinal cord injury identified before surgery. - METHODS: We conducted a retrospective study that included 57 patients who had experienced traumatic brachial plexus injuries and exhibited neuropathic pain that did not respond to conservative treatment methods. They were submitted to DREZ lesioning. We defined the inclusion and exclusion criteria, collected sociodemographic and clinical characteristics, and identified and classified spinal cord lesions based on magnetic resonance imaging. We applied statistical tests to evaluate the association between pain intensity after surgery and the radiological profile and sociodemographic characteristics. - RESULTS: Immediately after surgery, the pain outcome was considered good or excellent in 50 patients (89.28%). At the last follow-up, it was good or excellent in 39 patients (68.43%). There was no association (P > 0.05) between the pain outcome and the variables analyzed (time interval between trauma and DREZ lesioning, presence of spinal cord injury, age, the number of avulsed roots, and the type of pain). - CONCLUSIONS: DREZ lesioning using radiofrequency represents a significant therapeutic approach for managing neuropathic pain after a traumatic brachial plexus injury. - Key words - Brachial plexus avulsion - Dorsal root entry zone - Neuropathic pain - Surgery Abbreviations and Acronyms DREZ: Dorsal root entry zone MRI: Magnetic resonance imaging VAS: Visual analog scale e466 www.SCIENCEDIRECT.com Importantly, we found that the presence of a spinal cord injury is not associated with the surgical outcome. INTRODUCTION R esearchers have reported that 69%e95% of patients who experience traumatic brachial plexus injuries present with neuropathic pain.1-4 Depending on its intensity, neuropathic pain can be associated with depression and a lower quality of life,5-7 and it can be refractory to conservative treatment. In this situation, dorsal root entry zone (DREZ) lesioning can be indicated to treat neuropathic pain. There are different methods to perform DREZ lesioning, including ultrasound, laser, radiofrequency, and microsurgery.8 The clinical outcome after surgery is variable, and studies have reported a good prognosis in 60%e96% of cases.8-14 However, it is not clear what prognostic factors are responsible for this outcome variation because there are only a few studies on this subject.15 It has been suggested that the identification of spinal cord injury by magnetic resonance imaging (MRI) could indicate a worse prognosis after surgery.16 Our objectives were to report the surgical outcome after DREZ lesioning by radiofrequency and to analyze prognostic factors such as the presence of a spinal cord lesion. MATERIAL AND METHODS Study Design and Setting We conducted a retrospective study of 57 patients who attended our hospital from 2001 to 2020. The patients had experienced traumatic brachial plexus injuries and presented with neuropathic pain refractory to conservative treatment. The diagnosis of root avulsion was made primarily by clinical examination, MRI, From the 1Department of Neurological Surgery, Sarah Network of Rehabilitation Hospitals; and 2Department of Radiology, Sarah Network of Rehabilitation Hospitals, Brasilia, Brazil To whom correspondence should be addressed: Marcio de Mendonça Cardoso, M.Sc. [E-mail: [email protected]] Citation: World Neurosurg. (2023) 177:e466-e471. https://doi.org/10.1016/j.wneu.2023.06.077 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2023 Elsevier Inc. All rights reserved. WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2023.06.077 ORIGINAL ARTICLE MARCIO DE MENDONÇA CARDOSO ET AL. neurophysiological studies, and intraoperative analysis (in patients who had undergone brachial plexus reconstruction). We obtained data by reviewing electronic medical records. We followed the PROCESS Guidelines (https://www.processguideline.com) for this case series.17 Participants The inclusion criteria were the presence of a traumatic lesion of the brachial plexus with pain refractory to conservative treatment, submitted to DREZ lesioning, and age >18 years. The exclusion criteria were the use of other surgical procedures to treat pain besides DREZ lesioning, the absence of an outcome measure (a visual analog scale [VAS]) before or after surgery, and repeated DREZ lesioning. Our institution granted ethics approval, and we obtained informed consent from all patients. Variables We have reported the following sociodemographic and clinical characteristics: age, gender, and the time interval between trauma and DREZ lesioning. The patients reported their pain location and pain characteristics. Pain intensity was assessed using a VAS that ranged from 0 mm (no pain) to 100 mm (very intense pain). A member of the neurosurgical team was responsible for the pain evaluation. The VAS was applied immediately before surgery, every 6 months after surgery during the first 3 years, and every year thereafter. We defined pain outcomes after comparing the VAS score before surgery, immediately after surgery, and at the last follow-up visit. We categorized it as excellent (75% pain relief), good (50%e75% pain relief), or fair (<50% pain relief). We classified spinal cord lesions based on MRI. We considered exams to be normal if there was no evidence of abnormalities on axial T2 images of the spine. We classified lesions as: 1) focal if there was evidence of DREZ avulsion with a shallow abnormal signal of the dorsal horn; 2) extensive if there was evidence of an abnormal T2 signal with deep extension in the dorsal horn; or 3) diffuse if there was evidence of a lesion beyond the DREZ and Figure 1. Radiological classification of spinal cord lesions: (A) focal and superficial lesion identified in DREZ, classified as focal. (B) Focal lesion identified in DREZ, with deep extension, classified as extensive WORLD NEUROSURGERY 177: e466-e471, SEPTEMBER 2023 DORSAL ROOT ENTRY ZONE LESIONING dorsal horn (Figure 1). Two independent radiologists were responsible for the radiological evaluation. When there was not a consensus, a neurosurgeon participated in the evaluation and helped define the classification. Surgical complications were described when they occurred. Surgical Procedure The patient was placed in a prone position, and a Mayfield head holder was used. Hemilaminectomy from C5 to C7 or an open door laminoplasty (in patients with extensive arachnoiditis and spinal cord rotation, it was easier to identify the DREZ when we could also see the normal side) was performed. After opening the dura mater and arachnoid mater, the area of root avulsion was located. Radiofrequency thermocoagulation was performed with an electrode (75 C for 15 seconds). The electrode was inserted to a depth of 2 mm and angled 30e45 in the sagittal plane. A radiofrequency lesion was repeated every 1 mm in the area of the root avulsion. Motor- and somatosensory-evoked potentials were monitored during surgery. Two neurosurgeons performed the procedures. Statistical Analysis We used R version 4.2.0 for statistical analysis. We have presented the qualitative variables as absolute numbers and percentages and the quantitative variables as means and standard deviations. We evaluated the data for normality by using the Kolmogorove Smirnov test; only age had a normal distribution. When comparing the sociodemographic, clinical, and radiological profiles with the intensity and variation of pain, we applied the c2 and Wilcoxon signed-rank tests. We used Spearman correlation analysis to evaluate the relationship between pain variation before and after surgery with age, the time interval between trauma and surgery, and the number of avulsed roots. For all statistical tests, the significance level was 5%. lesion. (C) Lesion beyond the DREZ and dorsal horn and associated with ‘pitting’ of the left lateral part of the spinal cord classified as diffuse lesion. www.journals.elsevier.com/world-neurosurgery e467 ORIGINAL ARTICLE MARCIO DE MENDONÇA CARDOSO ET AL. DORSAL ROOT ENTRY ZONE LESIONING RESULTS The study included 57 patients, most of whom were men (55 patients). The mean VAS before surgery was 90.23. Pain was located exclusively in the forearm or hand in 34 patients (59.65%) (Table 1). The mean follow-up evaluation was 40.3 months (Table 1). The mean time interval between trauma and DREZ Table 1. Demographic and Clinical-Radiological Characteristics Variable Number of Patients (%) Sex Male 55 (96.49%) Female 2 (3.51%) Age 40 years 28 (49.12%) >40 years 29 (50.88%) Spinal cord injury* Yes 36 (72%) No 14 (28%) Radiological aspecty Extensive 24 (66.67%) Focal 10 (27.77%) Diffuse 2 (5.56%) Number of avulsed roots 3 25 (52.08%) >3 23 (47.92%) Location of avulsed roots C4 4 (8.33%) C5 20 (41.67%) C6 29 (60.42%) C7 41 (85.42%) C8 41 (85.42%) T1 33 (68.75%) Pain location Arm 1 (1.75%) Forearm-hand 18 (31.58%) Hand 16 (28.07) Whole arm 22 (38.60%) Pain characteristics Lancinating with paroxysms 1 (1.75%) Constant 32 (56.14%) Both lancinating and constant 24 (42.11%) *Diagnosed by magnetic resonance imaging. yRadiological classification described in the manuscript. e468 www.SCIENCEDIRECT.com lesioning was 66.9 months, and the median time interval was 46.5 months (range 7.1e363.6 months). Immediately after surgery, the pain outcome was considered good or excellent in 50 patients (89.28%). At the last follow-up evaluation, the pain outcome was good or excellent in 39 patients (68.43%) (Table 2). In this group, 26 patients did not take pain medication, whereas 13 did (gabapentin or amitriptyline). Based on MRI, 36 patients (63.16%) had a spinal cord lesion before surgery, 14 patients (24.56%) did not, and 7 patients (12.28%) did not have an adequate radiological evaluation and thus, we excluded them from this analysis. There was no association (P > 0.05) between the presence of a spinal cord lesion and the pain outcome after DREZ lesioning. There was no association between the pain outcome and variables such as age, the number of avulsed roots, or radiological aspect, as indicated in Table 3. Spearman’s correlation test, conducted at a significance level of 5%, revealed no significant difference between the pain outcome and the time interval between trauma and surgery (r (55) ¼ 0.05, P > 0.05). Furthermore, there was no significant correlation between the type of pain experienced before surgery and the subsequent relief of pain after the surgical intervention (P > 0.05). Immediately following the surgery, 8 patients (14.04%) reported motor paresis, while 13 (22.81%) patients reported various abnormalities or sensory deficits specifically affecting the ipsilateral lower limb. However, during the final follow-up evaluation, only 1 patient continued to experience motor paresis. It is noteworthy that this persistent motor paresis did not impact the patient’s ability to walk independently or necessitate any form of assistance. There were no general neurosurgical complications, such as infection or cerebrospinal fluid fistula. DISCUSSION The most common surgical techniques used for DREZ lesioning are radiofrequency and microsurgical lesioning using bipolar coagulation, as described by Nashold18 and Sindou.19 Previous studies indicate that to achieve a meaningful reduction in pain intensity after surgery, it is necessary to reduce the pain score (based on the VAS) by 30%e48%.20,21 Our surgical results demonstrate the increased relevance of DREZ lesioning in the treatment of refractory neuropathic pain, considering that most of our patients had pain relief (68.43% of the patients had a good or excellent outcome), and the incidence of severe neurological complications was small. Generally, neurological complications are caused by the entrance angle or depth of the radiofrequency needle in the spinal cord. When the inclination of the needle is small, there is a higher risk of lesioning the corticospinal tract. If the entrance point of the needle is located medially to the posterior-lateral sulcus of the spinal cord, then the posterior funiculus can be affected. In patients with extensive arachnoiditis and spinal cord retraction, finding the correct place for needle insertion can be very difficult. In this situation, it is important to release the spinal cord and to obtain a wider exposure to visualize the normal roots both above and below the affected area on the same side, as well as on the contralateral side. It is also important to control the temperature of the needle and the duration of the lesion. WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2023.06.077 ORIGINAL ARTICLE MARCIO DE MENDONÇA CARDOSO ET AL. DORSAL ROOT ENTRY ZONE LESIONING Table 2. Pain Comparison Before and After Surgery Variable Pain (VAS) before surgery Median (mm) Mean (mm) Standard Deviation P* 100.00 90.23 9.5 <0.001 Pain (VAS) immediately after surgery 0 10.16 20.11 Pain (VAS) variation before and immediately after surgery 90.00 80.54 24.60 Pain (VAS) at last follow-up visit 20.00 30.18 30.32 Pain (VAS) variation before surgery and at last follow-up visit 70.00 60.53 34.47 <0.001 VAS, visual analog scale. *Based on the Wilcoxon signed-rank test. that the absence of spinal cord injury associated with root avulsion before surgery was associated with important pain relief. The authors proposed that patients with a spinal cord injury have already had “DREZ lesioning” that occurred from the trauma. In this situation, neuropathic pain would be the result of altered activity at the supraspinal level.16 In our study, which has a larger sample than the study by Ko et al.,16 we did not observe this relationship, probably because there are other mechanisms besides hyperactive posterior horn neurons that could act together to influence neuropathic pain. First, it is important to consider that cortical reorganization is a well-established process that occurs after peripheral nerve injury. It is proposed that after brachial plexus injury, the corresponding cortical area is invaded by representations of the body parts adjacent to the missing limb, and this phenomenon may negatively influence motor recovery.24 Baruah et al.25 studied a series of patients before and after DREZ lesioning. Functional MRI was performed before and after surgery; they observed the development of cortical activation areas in patients with chronic It is crucial to highlight that pain relief at long-term follow-up may not be as effective as immediately after surgery, but it still represents a positive outcome when compared with other options like spinal cord stimulation.22 Analyzing the long-term outcomes after DREZ lesioning present challenges, primarily due to patient attrition. Many patients may choose to discontinue their participation in the study, especially if they live far from the hospital or have already experienced positive results from the procedure. This attrition can potentially introduce bias and limit the comprehensive assessment of long-term outcomes in DREZ lesioning studies. It has been suggested that neuropathic pain after traumatic brachial plexus root avulsion is caused by hyperactive posterior horn spinal cord neurons under the influence of a disinhibited lateral Lissauer tract. In line with this concept, DREZ lesioning has been adopted to treat refractory neuropathic pain because it will destroy these hyperactive neurons located in the posterior horn (Rexed lamina IeV).23 Considering this information, Ko et al.16 studied 17 patients after DREZ lesioning and observed Table 3. Association Between Pain Outcome at the Last Follow-Up Visiting and Demographic and Clinical-Radiological Characteristics Pain Outcome* Characteristics Excellent Good Fair Total Py 40 years 12 (42.86%) 6 (21.43%) 10 (35.71%) 28 (100%) 0.804 >40 years 14 (48.28%) 7 (24.14%) 8 (27.59%) 29 (100%) 3 13 (36.11%) 12 (33,33%) 2 (5.71%) 35 (100%) >3 9 (64.29%) 2 (14.29%) 3 (21.43%) 14 (100%) Absent 9 (64.29%) 2(14.29%) 3(21.43%) 14 (100%) Diffuse 2 (100%) — — 2 (100%) Extensive 8 (33.33%) 9 (37.50%) 7 (29.17%) 24 (100%) Focal 3 (30%) 2 (20%) 5 (50%) 10 (100%) Age Number of avulsed roots 0.190 Radiological aspect 0.191 *Number of patients (percentage). yc2. WORLD NEUROSURGERY 177: e466-e471, SEPTEMBER 2023 www.journals.elsevier.com/world-neurosurgery e469 ORIGINAL ARTICLE MARCIO DE MENDONÇA CARDOSO ET AL. DORSAL ROOT ENTRY ZONE LESIONING neuropathic pain, but after surgery, there was inactivation of this area in patients with pain relief. They suggested that the DREZ may send excitatory impulses to adjacent cortical areas.25 However, the mechanism by which brain plasticity influences neuropathic pain is controversial. Yanagisawa et al.26 used a brainemachine interface based on real-time magnetoencephalography signals to reconstruct affected hand movements with a robotic hand. They observed improved functional control of the amputated limb and hand prosthesis, but there was not consistent pain relief. A convergence among studies suggests that preventing abnormally increased or decreased activity in central areas by regulating sensory input and motor output signals may contribute to the treatment of neuropathic pain.27 Considering the currently available information concerning the relationship between cortical plasticity and pain, it is possible to find studies suggesting other treatment options for neuropathic pain: repetitive transcranial magnetic stimulation,28 mirror therapy, and cognitive behavioral therapy.29 We observed that during surgery, some patients had greater degeneration in the avulsion zone, characterized by the needle entering the spinal cord more loosely. In some cases, we noted the presence of microcysts. We hypothesize that under this circumstance, there is reduced propagation of heat, which consequently increases the risk of treatment failure. Unfortunately, we were unable to carry out this evaluation in our study because not all surgical reports presented an evaluation related to this aspect. The correlation between the number of avulsed roots and the pain outcome is a topic of ongoing debate and scientific inquiry. Piyawattanametha et al.15 conducted a study where they observed that fewer pain dermatomes were associated with a favorable prognosis following DREZotomy. However, comparing their findings with our own study is challenging due to differences in the patient inclusion criteria. Their study encompassed patients with neuropathic pain stemming from various etiologies such as trauma, tumors, and spinal cord injury, among others, while our study specifically focused on patients with brachial plexus injuries resulting from trauma. It is worth noting that many patients with flail arms experience pain primarily localized to the hand and forearm, despite presenting with multiple root avulsions. Consequently, the number of painful dermatomes does not consistently correlate with the number of root avulsions. In a separate investigation by Samii et al.,14 there was no significant correlation between the number of painful dermatomes and postoperative pain relief. We did not observe a significant association between pain relief and the time interval between trauma and DREZ lesioning. This finding is interesting because studies based on MRI indicate that regions related to memory and learning, such as the hippocampus and amygdala, are involved in chronic pain, which may explain treatment failure in some diseases such as back pain.30 We consider that a long interval between trauma and DREZ lesioning should not contraindicate surgery. It has been suggested that the type of pain before surgery could influence the pain outcome after surgery,10 but we did not observe this phenomenon in our study. Our findings strengthen our belief that the presence of persistent and intense burning e470 www.SCIENCEDIRECT.com pain should not be considered a contraindication for DREZ lesioning. Limitations Our study has a few limitations. First, it is retrospective and may have related bias, but it is important to consider that the previous study on the association between spinal cord injury and outcome after DREZ injury indicated a strong relationship.16 Therefore, considering the large effect size, the number of patients we evaluated may give us a better estimate of the presence or absence of an association. Second, we selected the laminectomy level according to Nashold,31 considering pain location, but not including T1 (because this spinal level originates at the T2 radicular filaments), and we cannot guarantee that a few patients had a worse prognosis because we did not include C4. Nevertheless, our surgical results are consistent with most of the medical literature on the topic.8 We should also mention that according to Sindou,10 the extent, in length, of the surgical lesioning was established based on pain topography, which generally corresponded with the avulsed segments as well as the altered adjacent rootlets, and in our study, no patient complained of pain that corresponded to C4 or C3; in fact, most of them indicated a pain location in the forearm and hand. Third, while grading pain using a VAS before and after surgery provides valuable information and is the most used scale for pain assessment, it would be beneficial to use scales that relate pain to functionality, such as the Brief Pain Inventory,32 for a more comprehensive assessment after surgery. Finally, we did not evaluate the presence of depression or secondary gain among the patients, despite the potential influence of these factors on the surgical prognosis. CONCLUSION DREZ lesioning using radiofrequency represents a significant therapeutic option for managing neuropathic pain resulting from a traumatic brachial plexus injury. This procedure often leads to pain relief, with rare occurrences of long-term neurological complications. Interestingly, our findings indicate that spinal cord injury, as diagnosed by MRI, and other variables examined in this study were not linked to the surgical outcome. This finding suggests the presence of additional factors beyond hyperactive neurons in the dorsal horn of the spinal cord that may contribute to neuropathic pain. Such factors may involve changes in cortical sensorimotor areas and brain plasticity after brachial plexus injury. Further investigation into these aspects is warranted to enhance our understanding of the complex mechanisms underlying neuropathic pain and to optimize treatment approaches. CRediT AUTHORSHIP CONTRIBUTION STATEMENT Marcio de Mendonça Cardoso: Conceptualization, Methodology, Writing e original draft, Visualization, Project administration. Ricardo Gepp: Writing e review & editing. Henrique Caetano: Writing e review & editing. Ricardo Felipe: Investigation, Data curation. Bernardo Martins: Data curation, Writing. WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2023.06.077 ORIGINAL ARTICLE MARCIO DE MENDONÇA CARDOSO ET AL. REFERENCES 1. Ciaramitaro P, Mondelli M, Logullo F, et al. Traumatic peripheral nerve injuries: epidemiological findings, neuropathic pain and quality of life in 158 patients. J Peripher Nerv Syst. 2010;15: 120-127. 2. Santana MVB, Bina MT, Paz MG, et al. High prevalence of neuropathic pain in the hand of patients with traumatic brachial plexus injury: a cross-sectional study. Arq Neuropsiquiatr. 2016;74: 895-901. 3. Tantigate D, Wongtrakul S, Vathana T, Limthongthang R, Songcharoen P. Neuropathic pain in brachial plexus injury. 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All rights reserved. www.journals.elsevier.com/world-neurosurgery e471