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Hand Surgery, Vol. 20, No. 1 (2015) 39–45 © World Scientific Publishing Company DOI: 10.1142/S0218810415500057
NEUROPATHIC PAIN IN BRACHIAL PLEXUS INJURY Direk Tantigate, Saichol Wongtrakul, Torpon Vathana, Roongsak Limthongthang and Panupan Songcharoen
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Department of Orthopaedic Surgery and Rehabilitation Faculty of Medicine, Siriraj Hospital Mahidol University, Bangkok 10700, Thailand Received 7 June 2014; Revised 3 September 2014; Accepted 4 September 2014; Published 20 January 2015 ABSTRACT Background: In Thailand, brachial plexus injury is a common traumatic injury that affects the function of the upper extremity. The current treatments focus mainly on improving the motor and sensory function. Apart from the motor and sensory deficit, these patients usually suffer from pain. Objective: The purpose of this study was to determine the prevalence and factors that relate to neuropathic pain in patients with brachial plexus injury. Methods: We collected data from March 2008 to July 2011. The DN4 Questionnaire was used to diagnose neuropathic pain in 95 patients. Results: The prevalence of neuropathic pain was as high as 76%. Majority of patients presented with hypoesthesia to pin prick, hypoesthesia to touch and numbness. Severity of neuropathic pain was significantly correlated with the type of brachial plexus injury. There was no difference between demographic characteristics of patients. Conclusion: Our study showed that the prevalence of neuropathic pain was high in brachial plexus injured patients. Therefore, surgeons should be aware of this common, yet underestimated, problem in brachial plexus injured patients. Keywords: Brachial Plexus Injury; Neuropathic Pain; Root Avulsion; Pain.
INTRODUCTION
shoulder abduction, elbow flexion and hand function have been reported.6,9,10 However, this severe disabling injury does not affect only on the physical functions but also psychological aspects from chronic pain. The exact mechanisms of this deafferentation pain are still unknown. The quality of life of brachial plexus injured patients may be worsed by chronic and intractable pain leading to unfavorable overall outcomes.11–13 Previous literatures have described a wide-ranging prevalence of neuropathic pain varying from very low to extremely high.4,14–25 Numerous factors including patient characteristics, type of injuries and environment were identified as the important factors in expression of pain. In this study, we prospectively evaluated 95
Brachial plexus injury is one of the common causes of the upper extremity disabling in Thailand. This injury is frequently caused by road traffic accidents especially motorcycle accidents.1 The current treatments target on restoring the upper extremity function to the pre-injury status as much as possible.2–4 For several decades, the management of brachial plexus injury has been improved with various types of reconstructive procedures, including nerve repair, nerve grafting, neurotization and functional free muscle transfer.5,6 These procedures mainly emphasize on recovering of the motor function and the protective sensation of the hand.7,8 Satisfactory outcomes of
Correspondence to: Dr. Panupan Songcharoen, Department of Orthopaedic Surgery and Rehabilitation, Faculty of Medicine, Siriraj Hospital, Mahidol University, Bangkok 10700, Thailand. Tel: (+66) 2-418-2215, Fax: (+66) 2-412-8172, E-mail: [email protected] 39
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brachial plexus injured patients. Our purpose was to identify the prevalence and the related factors of neuropathic pain in brachial plexus injured patients.
MATERIALS AND METHODS
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After the approval by the Institutional Review Board and obtaining an informed written consent, the data were collected regarding privacy and presentation assured confidentiality. Our study design was a cross-sectional study. All brachial plexus injured patients admitted for brachial plexus surgery during March 2008 to July 2011 were included in our study. Ninety-five patients over 18 years were included as the research targets. The patients who previously underwent brachial plexus surgery, or sustained brain injury, or had a psychiatric disorder or were enduring a chronic illness were excluded from this study. A standardised pain intensity scale, the Visual Analogue Scale (VAS), was used to evaluate patients with the symptoms of pain. Neuropathic pain was assessed by the clinician-administered Thai DN4 questionnaire, in correspondence to a total score of 4 or more out of 10. The accuracy of Thai DN4 questionnaire was proved by cross-cultural adaptation study with satisfying results.26 Demographic profiles including age, sex, dexterity, level of education and occupation such as sedentary, field worker and manual worker; which defined the occupation as requiring skilled work, were recorded. For injury-related data including date of injury, causes, associated injuries, type of brachial plexus injury (total arm type or incomplete type), cervical myelographic findings, timing of pain, environmental factors (surrounding temperature, activity) and treatment of pain were also recorded in the case record form. The quantitative data were analysed using mean and SD, while the qualitative data were analysed through figures and percentage scores. For statistical differences between the two groups, the quantitative data were analysed using the Student’s t-test (normality) or Mann–Whitney U-test (non-normality), while the qualitative data were analysed using the Chi-square test or Fisher’ exact test. A p-value of less than 0.05 was considered statistically significant. Statistical analysis was performed using the SPSS version 13 software program.
RESULTS From March 2008 to July 2011, we observed 95 patients with brachial plexus injury in our institute. Fifteen patients were
excluded because 10 patients previously underwent brachial plexus surgery and five patients had associated brain injury. Eighty patients were classified into two groups according to the pain score at the time of the first assessment. Group 1 (17 patients) included patients who had no pain (VAS ¼ 0) and group 2 (63 patients) included patients who had pain with varying degree (VAS > 0) (Fig. 1). After assessment with Thai DN4 questionnaire, it was found that 61 out of 63 patients suffered from neuropathic pain. Therefore, the prevalence of neuropathic pain in patients with brachial plexus injury was 76%. Our patients had a divergence of presentation of neuropathic pain such as numbness, electrical shocks and pin and needles sensation. For each presentation according to Thai DN4 questionnaire, the frequency is shown in Table 1. For the clinical features of the patients with neuropathic pain (Table 2), the mean VAS was as high as 4:91 2:38. Eighty-five percent of the patients developed neuropathic pain after six weeks of injury and 95% developed the pain in three months after injury. Thirty percent of them experienced the pain at night, while 56% had an uncertain time of symptoms. The environmental factors that aggravated the symptoms were cold temperature (39.3%) and movement of the affected limb (29.5%). For the treatment of neuropathic pain, 28 of 61 patients (45.9%) had received one or more medications including paracetamol, NSAIDs, tramadol, tricyclic antidepressant and gabapentin. According to the assessment of the medications given to the patients with neuropathic pain, tricyclic antidepressant was the most common drug used and the second was gabapentin. Unfortunately, 33 of 61 patients (54.1%) had not received any medications. Further study by subgroup analysis in patients with neuropathic pain revealed significant correlation between types of brachial plexus injury and the severity of neuropathic pain (Table 3). The patients who sustained total arm type brachial plexus injury, defined as all roots involvement, suffered more severe pain (VAS > 6) than the patients who sustained incomplete injury, defined as some roots involvement. By comparing of VAS between the treated and untreated groups of patients with neuropathic pain, there was no significant difference in the intensity of pain. Surprisingly, the range of VAS between both groups was nearly the same (Table 4). For studying the factors that affected the neuropathic pain, 14 patients of group 1 (VAS ¼ 0) were compared with 61
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Fig. 1 Schematic data demonstrated groups of patients according to symptoms and types of pain and subdivided into treated and untreated groups. (BPI: brachial plexus injury, NeP: neuropathic pain.)
Table 1
Frequency of Each Item in Thai DN4 Questionnaire. Yes
No
Does the pain have one or more of the following characteristics? Burning 23 (37.7%) 38 (62.3%) Painful cold 17 (27.9%) 44 (72.1%) Electric shocks 45 (73.8%) 16 (26.2%) Is the pain associated with one or more of the following questions in the same area? Tingling 43 (70.5%) 18 (29.5%) Pins and needles 44 (72.1%) 17 (27.9%) Numbness 54 (88.5%) 7 (11.5%) Itching 19 (31.1%) 42 (68.9%) Is the pain located in an area where the physical examination may reveal one or more of the following characteristics? Hypoesthesia to touch 55 (90.2%) 6 (9.8%) Hypoestesia to prick 56 (91.8%) 5 (8.2%) In the pain area, can the pain be caused by or increased by: Brushing 12 (19.7%) 49 (80.3%)
patients with neuropathic pain of group 2 (VAS > 0). Three patients of group 1 who received pain medication at the time of the first assessment were not included because there was no cause of pain in these patients. The demographic data of two groups are summarized in Table 5. There was no significant difference between the patient characteristics. However, the patients with neuropathic pain tended to change their occupation to sedentary life after sustaining the injury. There were
Table 2 Clinical Features of 61 Brachial Plexus Injured Patients Suffered with Neuropathic Pain. Pain severity VAS Onset of symptom Within 6 weeks 6 weeks–3 months 3–6 months >6 months Timing of symptom Morning Afternoon Evening Night Uncertain Environmental factor Climate-Cold -Hot -Uncertain Activity-Aggravating pain -No change -Uncertain Treatment No medication Medication a Paracetamol NSAIDs Tramadol Tricyclic antidepressant Gabapentin a These
4:91 2:38 (1–10) 52 6 2 1
(85.2%) (9.8%) (3.3%) (1.6%)
6 1 2 18 34
(9.8%) (1.6%) (3.3%) (29.5%) (55.7%)
24 1 36 18 30 13
(39.3%) (1.6%) (59.0%) (29.5%) (49.2%) (21.3%)
33 (54.1%) 28 (45.9%) 11 6 11 15 13
patients might have received more than 1 medication.
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Table 3 Correlation Between Types of Injury and VAS of the Patients with Neuropathic Pain.
Type of injury Incomplete type Total arm type
VAS < 4 (n = 22)
VAS 4–6 (n---24)
VAS > 6 (n = 15)
15 7
10 14
4 11
Group I (No Pain) (n = 14, M = 14)
0.035 a Age (yrs)
Table 4 Comparison of VAS of Treated and Untreated Patients with Neuropathic Pain.
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Demographic Data of 75 Patients with Brachial Plexus
p-value
For statistical analysis: a Chi square test.
VAS score Mean SD Min–Max
Table 5 Injury.
Without Medication (n = 33)
With Medication (n = 28)
4:47 2:06 1.6–10.0
5:44 2:66 1.0–10.0
p-value 0.11 a
For statistical analysis: a Student’s t-test.
no significant differences of the injury related factors including causes, types of injury and cervical myelographic findings between these two groups.
DISCUSSION Brachial plexus injury is a common traumatic neuropathy of the upper extremity. Mostly, this injury occurs in young and working age groups. The injury does not affect only the patients’ occupation but also their whole lifestyles. This severe disabling injury involves both patients’ physical and psychological well-being. The treatment with various procedures is mainly emphasized on restoring motor and sensory functions.2,3,6–8 Apart from recovery of motor and sensory functions, pain or psychological aspect plays an important role in overall outcomes. For example, some patients stated that recovery of motor power to grade MRC 3 may be merely of academic interest if the limb is too painful to use. Some literatures19,27 reported that general life satisfaction of patients was not significantly affected by the level of function of the upper limb. However, Ciaramitaro et al.20 demonstrated that severity of pain especially moderate and severe pain was strongly associated with impairment in the quality of life. The prevalence of pain in brachial plexus injured patients was reported by previous literatures varying from 20% to 95%.4,14–25 However, most of these studies retrospectively
Dominant hand Right Left Education Higher level of high school Lower level of high school Occupation: Prior to injury Manual worker Field worker Occupation: Post injury Sedentary Worker –Manual worker –Field worker Causes of injury Motorcycle accident Fall Others (gun shot, car accident, Stab wound) Type of injury Incomplete upper arm type Complete type Cervical myelographic finding Pseudomeningocele Abnormal root Normal Not done
Group II (Neuropathic Pain) (n = 61, M = 57, F = 4) p-value
28:36 7:68 28:72 10:32 (18–42 yrs) (18–62 yrs)
0.90 b
11 (78.6%) 3 (21.4%)
53 (86.9%) 8 (13.1%)
0.42 a
4 (28.6%) 10 (71.4%)
16 (26.2%) 45 (73.8%)
0.99 a
6 (42.9%) 8 (57.1%)
35 (57.4%) 26 (42.6%)
0.33 a
8 (57.1%) 6 (42.9%) 5 1
48 (78.7%) 13 (21.3%) 9 4
11 (78.6%) 2 (14.3%) 1 (7.1%)
55 (90.2%) 3 (4.9%) 3 (4.9%)
8 (57.1%) 6 (42.9%)
29 (47.5%) 32 (52.5%)
7 (50.0%) 5 (35.7%) 2 (14.3%)
35 18 2 6
0.17 a
0.52 a
(57.4%) (29.5%) (3.3%) (9.8%)
For statistical analysis: a Fisher’s exact test/Chi-square test, b Student’s t-test, c Mann–Whitney U-test.
reviewed the patients who underwent both conservative and operative treatments. Recent literatures demonstrated that the successful surgical repair was associated with pain relief.15,16,21 Therefore, the patients who underwent any kinds of brachial plexus surgery were excluded from our study. The characteristic of pain from previous literatures was described by several terms such as burning, crushing, and shooting or electric shock. Some patients even explained their symptom as \pin and needle" or \putting your fingers in a socket and somebody switching the socket on and off".13 However, the specific cause
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of pain was not defined by these studies. Finnerup et al.28 created a new tool named McGill Pain Questionnaire (MPQ) to assess the characteristic of pain. They revealed that the most common pain descriptors were shooting, penetrating, tingling, exhausting, and agonizing. It is believed that all brachial plexus injured patients would suffer from neuropathic pain which is the pain resulting from a primary lesion or dysfunction of the nervous system. However, Ciaramitaro et al.20 reported that only 67% of patients sustained brachial plexus injury experienced neuropathic pain. The remaining patients suffered from other kinds of pain termed as non-neuropathic pain. The clinical significance of neuropathic pain has been proposed in many literatures. Neuropathic pain is more chronic with stronger cognitive modulation than nociceptive pain. The response to specific classes of pain medications leads the physicians to get an accurate diagnosis between neuropathic or non-neuropathic pain. A new validated screening tool entitled Douleur Neuropathique en 4 questions (DN4) has also been developed and accepted as the standard tool for diagnosing neuropathic pain. The DN4 comprises seven items related to symptoms and three items related to clinical examination. The prevalence of neuropathic pain diagnosed by the DN4 varied from 67–95%.20,25 The sensitivity and specificity of the DN4 were 83% and 90% respectively compared to the clinical diagnosis of neuropathic pain.29 According to the DN4 questionnaire, Vanier et al.25 found that 95% of 60 brachial plexus injured patients suffered from neuropathic pain. Seventy five percent of these patients received the medical treatments, however, only 37% of the treated patients were satisfied with the outcomes of treatment. Ciaramitaro et al.20 evaluated 158 patients with traumatic peripheral nerve injury from four centres in Italy. Seventy-six patients had brachial plexus injury, which classified as brachial plexopathy in 54 patients and root avulsion injury in 22 patients. According to the DN4 questionnaire, the incidences of neuropathic pain in brachial plexus injured patients was 67%. Interestingly, all patients who had root avulsion injury suffered from neuropathic pain. Similar to our study, 97% of patients with brachial plexus injury experienced pain, and the incidence of neuropathic pain in these patients was as high as 76%. Eighty-five percent of neuropathic pain occurred within six weeks after injury, which was comparable to the previous study.18 The pathophysiology of neuropathic pain in brachial plexus injured patients was root avulsion and spinal cord
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deafferentation,11,17,20,30 non-avulsed root17,31 or cortical sensitisation.12,19,32 The treatment strategy ranged from empirical drug therapy, nerve transfer surgery and dorsal root entry zone (DREZ) surgery depending on severity of the pain.16,33,34 Medical treatment of neuropathic pain has recently been based on the recommendation of general practice guidelines developed from the majority of large randomized controlled trial including diabetes neuropathy and post herpetic neuralgia. The existing guidelines35,36 have not specified patients with brachial plexus injury and have a small body of evidence in treating neuropathic pain caused by brachial plexus injury.37 Medications, which have proved efficacy in treating different neuropathic pain conditions, may have the probability of being useful in additional conditions.38 However, it is possible that some neuropathic pain conditions may respond differently to the recommended treatment.39 By analyzing the medical treatment of neuropathic pain in our study, there were different analgesic treatment strategies from referring hospitals. The commonly prescribed medications were tricyclic antidepressant, gabapentin and tramadol, respectively. Similarly to previous literatures, medications given to our patients were the first line drugs of neuropathic pain treatment.18,25 Interestingly, more than half of the patients who had experienced pain did not receive any medications. These might probably be caused by lack of information, inexperience in severe disabling injury and underestimation of the pain. In a further evaluation of the intensity of pain between the treated and untreated group, the results demonstrated that there were no significant differences of VAS between both groups. Many factors may contribute to these outcomes including compliance, response to treatment, reassessment and dose adjustment. Factors related to neuropathic pain have been proposed in earlier literatures including severity and extent of injury. The significant correlation between pain intensity and the number of root avulsion was also demonstrated.18,21 In our study, there was significant correlation between types of brachial injury, classified as incomplete or compete injury according to numbers of root involvement, and the severity of neuropathic pain according to visual analogue scale. Root avulsion could be the major cause of the neuropathic pain. However, some authors proposed the conflicting data that non-avulsed roots had a possible role in pain generation.40 Diagnosis of root avulsion can be made by physical examination, cervical myelography, perioperative electrophysiology and direct intraoperative inspection of the exposed brachial plexus (if applicable).
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Myelographic findings were used to define the type of nerve root injury in our study. The results showed no correlation between myelographic findings and neuropathic pain. Environmental factors such as cold temperature and physical contact have been described as aggravating factors.39 In our study, we found no significant correlation between environmental factors and neuropathic pain. Because our study was carried out in the tertiary centre, where the severe injuries were predominant and might contribute to the selection bias, patients with neurapraxia that might improve without nerve surgery were not included.
CONCLUSION Hand Surg. 2015.20:39-45. Downloaded from www.worldscientific.com by FUDAN UNIVERSITY on 05/02/15. For personal use only.
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Neuropathic pain occurring in patients that have sustained a brachial plexus injury is commonly overlooked and underestimated, despite the 76% of incidence, resulting in reducing the overall outcomes even though the successful motor function recovery of the affected limb is possible. Clinicians should have high index of suspicion and must be careful in evaluating the neuropathic pain with both VAS and the screening tool (DN4) and treating this pain with the appropriate classes of pain medication to attain better quality of life in such patients.
ACKNOWLEDGEMENTS We would like to express our great appreciation to Dr. Pongparadee Chaudakshetrin for her valuable and constructive suggestions during the planning and development of this research work. Her willingness to give her time so generously has been very much appreciated. We would also like to extend our thanks to Narumol Sudjai for her help in offering us the statistical analysis of the results. All investigators have no conflict of interest.
References 1. Songcharoen P, Brachial plexus injury in Thailand: A report of 520 cases, Microsurgery 16:35–39, 1995. 2. Giuffre JL, Kakar S, Bishop AT, Spinner RJ, Shin AY, Current concepts of the treatment of adult brachial plexus injuries, J Hand Surg Am 35:678–688, 2010. 3. Songcharoen P, Management of brachial plexus injury in adults, Scand J Surg 97:317–323, 2008. 4. Terzis JK, Kostopoulos VK, The surgical treatment of brachial plexus injuries in adults, Plast Reconstr Surg 119:73e–92e, 2007.
5. Yang LJS, Chang KWC, Chung KC, A systematic review of nerve transfer and nerve repair for the treatment of adult upper brachial plexus injury, Neurosurgery 71:417–429, 2012. 6. Doi K, Muramatsu K, Hattori Y, Otsuka K, Tan S-H, Nanda V, Watanabe M, Restoration of prehension with the double free muscle technique following complete avulsion of the brachial plexus indications and longterm results, J Bone Joint Surg Am 82:652–666, 2000. 7. Hattori Y, Doi K, Sakamoto S, Yukata K, Sensory recovery of the hand with intercostal nerve transfer following complete avulsion of the brachial plexus, Plast Reconstr Surg 123:276–283, 2009. 8. Songcharoen P, Wongtrakul S, Mahaisavariya B, Spinner RJ, Hemicontralateral C7 transfer to median nerve in the treatment of root avulsion brachial plexus injury, J Hand Surg Am 26:1058–1064, 2001. 9. Merrell GA, Barrie KA, Katz DL, Wolfe SW, Results of nerve transfer techniques for restoration of shoulder and elbow function in the context of a meta-analysis of the English literature, J Hand Surg Am 26:303– 314, 2001. 10. Sulaiman OAR, Kim DD, Burkett C, Kline DG, Nerve transfer surgery for adult brachial plexus injury, Neurosurgery 65:A55–A62, 2009. 11. Ahmed-Labib M, Golan JD, Jacques L, Functional outcome of brachial plexus reconstruction after trauma, Neurosurgery 61:1016–1013, 2007. 12. Wellington B, Quality of life issues for patients following traumatic brachial plexus injury — Part 1 A Literature review, Int J Orthop Trauma Nursing 13:194–200, 2009. 13. Wellington B, Quality of life issues for patients following traumatic brachial plexus injury — Part 2 research project, Int J Orthop Trauma Nursing 14:5–11, 2010. 14. Bentolila V, Nizard R, Bizot P, Sedel L, Complete traumatic brachial plexus palsy. Treatment and outcome after repair, J Bone Joint Surg Am 81:20–28, 1999. 15. Berman J, Anand P, Chen L, Taggart M, Birch R, Pain relief from preganglionic injury to the brachial plexus by late intercostal nerve transfer, J Bone Joint Surg Br 78:759–760, 1996. 16. Berman J, Birch R, Anand P, Pain following human brachial plexus injury with spinal cord root avulsion and the effect of surgery, Pain 75:199–207, 1998. 17. Bertelli JA, Ghizoni MF, LoureIro Chaves DP, Sensory disturbances and pain complaints after brachial plexus root injury: A prospective study involving 150 adult patients, Microsurgery 31:93–97, 2010. 18. Bruxelle J, Travers V, Thiebaut JB, Occurrence and treatment of pain after brachial plexus injury, Clin Orthop Relat Res 237:87–95, 1988. 19. Choi PD, Novak CB, Mackinnon SE, Kline DG, Quality of life and functional outcome following brachial plexus injury, J Hand Surg Am 22:605–612, 1997. 20. Ciaramitaro P, Mondelli M, Logullo F, Grimaldi S, Battiston B, Sard A, Scarinzi C, Migliaretti G, Faccani G, Cocito D, Traumatic peripheral nerve injuries: Epidemiological findings, neuropathic pain and quality of life in 158 patients, J Peripher Nerv Syst 15:120–127, 2010. 21. Htut M, Misra P, Anand P, Birch R, Carlstedt T, Pain phenomena and sensory recovery following brachial plexus avulsion injury and surgical repairs, J Hand Surg Br 31:596–605, 2006.
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22. Kretschmer T, Ihle S, Antoniadis G, Seidel JA, Heinen C, B€orm W, Richter H-P, K€onig R, Patient satisfaction and disability after brachial plexus surgery, Neurosurgery 65:A189–A196, 2009. 23. Lusskin R, Campbell JB, Thompson WA, Post-traumatic lesions of the brachial plexus: Treatment by transclavicular exploration and neurolysis or autograft reconstruction, J Bone Joint Surg Am 55:1159–1176, 1973. 24. Narakas AO, Hentz VR, Neurotization in brachial plexus injuries. Indication and results, Clin Orthop Relat Res 237:43–56, 1988. 25. Vannier JL, Belkheyar Z, Oberlin C, Montravers P, Prise en charge des douleursneuropathiques des lesionstraumatiques du plexus brachial chez l’adulte. À propos de 60 cas, Ann Fr Anesth Reanim 27:890–895, 2008. 26. Chaudakshetrin P, Prateepavanich P, Chira-Adisai W, Tassanawipas W, Leechavengvongs S, Kitisomprayoonkul W, Cross-cultural adaptation to the Thai language of the neuropathic pain diagnostic questionnaire (DN4), J Med Assoc Thai 90:1860–1865, 2007. 27. Bailey R, Kaskutas V, Fox I, Baum CM, Mackinnon SE, Effect of upper extremity nerve damage on activity participation, pain, depression, and quality of life, J Hand Surg Am 34:1682–1688, 2009. 28. Finnerup NB, Norrbrink C, Fuglsang-Frederiksen A, Terkelsen AJ, Hojlund AP, Jensen TS, Pain, referred sensations, and involuntary muscle movements in brachial plexus injury, Acta Neurol Scand 121:320–327, 2010. 29. Cruccu G, Anand P, Attal N, Garcia-Larrea L, Haanpää M, Jørum E, Serra J, Jensen TS, EFNS guidelines on neuropathic pain assessment, Eur J Neurol 11:153–162, 2004. 30. Campbell JNJ, Meyer RAR, Mechanisms of neuropathic pain, Neuron 52:77–92, 2006. 31. Bertelli JA, Ghizoni MF, Pain after avulsion injuries and complete palsy of the brachial plexus: The possible role of nonavulsed roots in pain generation, Neurosurgery 62:1104–1114, 2008.
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32. Lu VB, Ballanyi K, Colmers WF, Smith PA, Neuron type-specific effects of brain-derived neurotrophic factor in rat superficial dorsal horn and their relevance to ‘central sensitization’, J Physiol 584:543–563, 2007. 33. Samii M, Bear-Henney S, Lüdemann W, Tatagiba M, Bl€omer U, Treatment of refractory pain after brachial plexus avulsion with dorsal root entry zone lesions, Neurosurgery 48:1269–1267, 2001. 34. Thomas DG, Kitchen ND, Long-term follow up of dorsal root entry zone lesions in brachial plexus avulsion, J Neurol Neurosurg Psychiatry 57:737–738, 1994. 35. Attal N, Cruccu G, Baron R, Haanpää M, Hansson P, Jensen TS, Nurmikko T, EFNS guidelines on the pharmacological treatment of neuropathic pain: 2010 revision, Eur J Neurol 17:1113–1188, 2010. 36. Dworkin RH, O’Connor AB, Backonja M, Farrar JT, Finnerup NB, Jensen TS, Kalso EA, Loeser JD, Miaskowski C, Nurmikko TJ, Portenoy RK, Rice ASC, Stacey BR, Treede R-D, Turk DC, Wallace MS, Pharmacologic management of neuropathic pain: Evidence-based recommendations, Pain 132:237–251, 2007. 37. Berman J, Symonds C, Birch R, Efficacy of two cannabis based medicinal extracts for relief of central neuropathic pain from brachial plexus avulsion: Results of a randomised controlled trial, Pain 112:299–306, 2004. 38. Hansson PT, Dickenson AH, Pharmacological treatment of peripheral neuropathic pain conditions based on shared commonalities despite multiple etiologies, Pain 113:251–254, 2005. 39. Attal N, Cruccu G, Haanpää M, Hansson P, Jensen TS, Nurmikko T, Sampaio C, Sindrup S, Wiffen P, EFNS guidelines on pharmacological treatment of neuropathic pain, Eur J Neurol 13:1153–1169, 2006. 40. Bertelli JA, Ghizoni MF, The possible role of regenerating axons in pain persistence after brachial plexus grafting, Microsurgery 30:532–536, 2010.
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Hand Surgery, Vol. 20, No. 1 (2015) 39–45 © World Scientific Publishing Company DOI: 10.1142/S0218810415500057
NEUROPATHIC PAIN IN BRACHIAL PLEXUS INJURY Direk Tantigate, Saichol Wongtrakul, Torpon Vathana, Roongsak Limthongthang and Panupan Songcharoen
Hand Surg. 2015.20:39-45. Downloaded from www.worldscientific.com by FUDAN UNIVERSITY on 05/02/15. For personal use only.
Department of Orthopaedic Surgery and Rehabilitation Faculty of Medicine, Siriraj Hospital Mahidol University, Bangkok 10700, Thailand Received 7 June 2014; Revised 3 September 2014; Accepted 4 September 2014; Published 20 January 2015 ABSTRACT Background: In Thailand, brachial plexus injury is a common traumatic injury that affects the function of the upper extremity. The current treatments focus mainly on improving the motor and sensory function. Apart from the motor and sensory deficit, these patients usually suffer from pain. Objective: The purpose of this study was to determine the prevalence and factors that relate to neuropathic pain in patients with brachial plexus injury. Methods: We collected data from March 2008 to July 2011. The DN4 Questionnaire was used to diagnose neuropathic pain in 95 patients. Results: The prevalence of neuropathic pain was as high as 76%. Majority of patients presented with hypoesthesia to pin prick, hypoesthesia to touch and numbness. Severity of neuropathic pain was significantly correlated with the type of brachial plexus injury. There was no difference between demographic characteristics of patients. Conclusion: Our study showed that the prevalence of neuropathic pain was high in brachial plexus injured patients. Therefore, surgeons should be aware of this common, yet underestimated, problem in brachial plexus injured patients. Keywords: Brachial Plexus Injury; Neuropathic Pain; Root Avulsion; Pain.
INTRODUCTION
shoulder abduction, elbow flexion and hand function have been reported.6,9,10 However, this severe disabling injury does not affect only on the physical functions but also psychological aspects from chronic pain. The exact mechanisms of this deafferentation pain are still unknown. The quality of life of brachial plexus injured patients may be worsed by chronic and intractable pain leading to unfavorable overall outcomes.11–13 Previous literatures have described a wide-ranging prevalence of neuropathic pain varying from very low to extremely high.4,14–25 Numerous factors including patient characteristics, type of injuries and environment were identified as the important factors in expression of pain. In this study, we prospectively evaluated 95
Brachial plexus injury is one of the common causes of the upper extremity disabling in Thailand. This injury is frequently caused by road traffic accidents especially motorcycle accidents.1 The current treatments target on restoring the upper extremity function to the pre-injury status as much as possible.2–4 For several decades, the management of brachial plexus injury has been improved with various types of reconstructive procedures, including nerve repair, nerve grafting, neurotization and functional free muscle transfer.5,6 These procedures mainly emphasize on recovering of the motor function and the protective sensation of the hand.7,8 Satisfactory outcomes of
Correspondence to: Dr. Panupan Songcharoen, Department of Orthopaedic Surgery and Rehabilitation, Faculty of Medicine, Siriraj Hospital, Mahidol University, Bangkok 10700, Thailand. Tel: (+66) 2-418-2215, Fax: (+66) 2-412-8172, E-mail: [email protected] 39
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brachial plexus injured patients. Our purpose was to identify the prevalence and the related factors of neuropathic pain in brachial plexus injured patients.
MATERIALS AND METHODS
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After the approval by the Institutional Review Board and obtaining an informed written consent, the data were collected regarding privacy and presentation assured confidentiality. Our study design was a cross-sectional study. All brachial plexus injured patients admitted for brachial plexus surgery during March 2008 to July 2011 were included in our study. Ninety-five patients over 18 years were included as the research targets. The patients who previously underwent brachial plexus surgery, or sustained brain injury, or had a psychiatric disorder or were enduring a chronic illness were excluded from this study. A standardised pain intensity scale, the Visual Analogue Scale (VAS), was used to evaluate patients with the symptoms of pain. Neuropathic pain was assessed by the clinician-administered Thai DN4 questionnaire, in correspondence to a total score of 4 or more out of 10. The accuracy of Thai DN4 questionnaire was proved by cross-cultural adaptation study with satisfying results.26 Demographic profiles including age, sex, dexterity, level of education and occupation such as sedentary, field worker and manual worker; which defined the occupation as requiring skilled work, were recorded. For injury-related data including date of injury, causes, associated injuries, type of brachial plexus injury (total arm type or incomplete type), cervical myelographic findings, timing of pain, environmental factors (surrounding temperature, activity) and treatment of pain were also recorded in the case record form. The quantitative data were analysed using mean and SD, while the qualitative data were analysed through figures and percentage scores. For statistical differences between the two groups, the quantitative data were analysed using the Student’s t-test (normality) or Mann–Whitney U-test (non-normality), while the qualitative data were analysed using the Chi-square test or Fisher’ exact test. A p-value of less than 0.05 was considered statistically significant. Statistical analysis was performed using the SPSS version 13 software program.
RESULTS From March 2008 to July 2011, we observed 95 patients with brachial plexus injury in our institute. Fifteen patients were
excluded because 10 patients previously underwent brachial plexus surgery and five patients had associated brain injury. Eighty patients were classified into two groups according to the pain score at the time of the first assessment. Group 1 (17 patients) included patients who had no pain (VAS ¼ 0) and group 2 (63 patients) included patients who had pain with varying degree (VAS > 0) (Fig. 1). After assessment with Thai DN4 questionnaire, it was found that 61 out of 63 patients suffered from neuropathic pain. Therefore, the prevalence of neuropathic pain in patients with brachial plexus injury was 76%. Our patients had a divergence of presentation of neuropathic pain such as numbness, electrical shocks and pin and needles sensation. For each presentation according to Thai DN4 questionnaire, the frequency is shown in Table 1. For the clinical features of the patients with neuropathic pain (Table 2), the mean VAS was as high as 4:91 2:38. Eighty-five percent of the patients developed neuropathic pain after six weeks of injury and 95% developed the pain in three months after injury. Thirty percent of them experienced the pain at night, while 56% had an uncertain time of symptoms. The environmental factors that aggravated the symptoms were cold temperature (39.3%) and movement of the affected limb (29.5%). For the treatment of neuropathic pain, 28 of 61 patients (45.9%) had received one or more medications including paracetamol, NSAIDs, tramadol, tricyclic antidepressant and gabapentin. According to the assessment of the medications given to the patients with neuropathic pain, tricyclic antidepressant was the most common drug used and the second was gabapentin. Unfortunately, 33 of 61 patients (54.1%) had not received any medications. Further study by subgroup analysis in patients with neuropathic pain revealed significant correlation between types of brachial plexus injury and the severity of neuropathic pain (Table 3). The patients who sustained total arm type brachial plexus injury, defined as all roots involvement, suffered more severe pain (VAS > 6) than the patients who sustained incomplete injury, defined as some roots involvement. By comparing of VAS between the treated and untreated groups of patients with neuropathic pain, there was no significant difference in the intensity of pain. Surprisingly, the range of VAS between both groups was nearly the same (Table 4). For studying the factors that affected the neuropathic pain, 14 patients of group 1 (VAS ¼ 0) were compared with 61
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Fig. 1 Schematic data demonstrated groups of patients according to symptoms and types of pain and subdivided into treated and untreated groups. (BPI: brachial plexus injury, NeP: neuropathic pain.)
Table 1
Frequency of Each Item in Thai DN4 Questionnaire. Yes
No
Does the pain have one or more of the following characteristics? Burning 23 (37.7%) 38 (62.3%) Painful cold 17 (27.9%) 44 (72.1%) Electric shocks 45 (73.8%) 16 (26.2%) Is the pain associated with one or more of the following questions in the same area? Tingling 43 (70.5%) 18 (29.5%) Pins and needles 44 (72.1%) 17 (27.9%) Numbness 54 (88.5%) 7 (11.5%) Itching 19 (31.1%) 42 (68.9%) Is the pain located in an area where the physical examination may reveal one or more of the following characteristics? Hypoesthesia to touch 55 (90.2%) 6 (9.8%) Hypoestesia to prick 56 (91.8%) 5 (8.2%) In the pain area, can the pain be caused by or increased by: Brushing 12 (19.7%) 49 (80.3%)
patients with neuropathic pain of group 2 (VAS > 0). Three patients of group 1 who received pain medication at the time of the first assessment were not included because there was no cause of pain in these patients. The demographic data of two groups are summarized in Table 5. There was no significant difference between the patient characteristics. However, the patients with neuropathic pain tended to change their occupation to sedentary life after sustaining the injury. There were
Table 2 Clinical Features of 61 Brachial Plexus Injured Patients Suffered with Neuropathic Pain. Pain severity VAS Onset of symptom Within 6 weeks 6 weeks–3 months 3–6 months >6 months Timing of symptom Morning Afternoon Evening Night Uncertain Environmental factor Climate-Cold -Hot -Uncertain Activity-Aggravating pain -No change -Uncertain Treatment No medication Medication a Paracetamol NSAIDs Tramadol Tricyclic antidepressant Gabapentin a These
4:91 2:38 (1–10) 52 6 2 1
(85.2%) (9.8%) (3.3%) (1.6%)
6 1 2 18 34
(9.8%) (1.6%) (3.3%) (29.5%) (55.7%)
24 1 36 18 30 13
(39.3%) (1.6%) (59.0%) (29.5%) (49.2%) (21.3%)
33 (54.1%) 28 (45.9%) 11 6 11 15 13
patients might have received more than 1 medication.
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Table 3 Correlation Between Types of Injury and VAS of the Patients with Neuropathic Pain.
Type of injury Incomplete type Total arm type
VAS < 4 (n = 22)
VAS 4–6 (n---24)
VAS > 6 (n = 15)
15 7
10 14
4 11
Group I (No Pain) (n = 14, M = 14)
0.035 a Age (yrs)
Table 4 Comparison of VAS of Treated and Untreated Patients with Neuropathic Pain.
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Demographic Data of 75 Patients with Brachial Plexus
p-value
For statistical analysis: a Chi square test.
VAS score Mean SD Min–Max
Table 5 Injury.
Without Medication (n = 33)
With Medication (n = 28)
4:47 2:06 1.6–10.0
5:44 2:66 1.0–10.0
p-value 0.11 a
For statistical analysis: a Student’s t-test.
no significant differences of the injury related factors including causes, types of injury and cervical myelographic findings between these two groups.
DISCUSSION Brachial plexus injury is a common traumatic neuropathy of the upper extremity. Mostly, this injury occurs in young and working age groups. The injury does not affect only the patients’ occupation but also their whole lifestyles. This severe disabling injury involves both patients’ physical and psychological well-being. The treatment with various procedures is mainly emphasized on restoring motor and sensory functions.2,3,6–8 Apart from recovery of motor and sensory functions, pain or psychological aspect plays an important role in overall outcomes. For example, some patients stated that recovery of motor power to grade MRC 3 may be merely of academic interest if the limb is too painful to use. Some literatures19,27 reported that general life satisfaction of patients was not significantly affected by the level of function of the upper limb. However, Ciaramitaro et al.20 demonstrated that severity of pain especially moderate and severe pain was strongly associated with impairment in the quality of life. The prevalence of pain in brachial plexus injured patients was reported by previous literatures varying from 20% to 95%.4,14–25 However, most of these studies retrospectively
Dominant hand Right Left Education Higher level of high school Lower level of high school Occupation: Prior to injury Manual worker Field worker Occupation: Post injury Sedentary Worker –Manual worker –Field worker Causes of injury Motorcycle accident Fall Others (gun shot, car accident, Stab wound) Type of injury Incomplete upper arm type Complete type Cervical myelographic finding Pseudomeningocele Abnormal root Normal Not done
Group II (Neuropathic Pain) (n = 61, M = 57, F = 4) p-value
28:36 7:68 28:72 10:32 (18–42 yrs) (18–62 yrs)
0.90 b
11 (78.6%) 3 (21.4%)
53 (86.9%) 8 (13.1%)
0.42 a
4 (28.6%) 10 (71.4%)
16 (26.2%) 45 (73.8%)
0.99 a
6 (42.9%) 8 (57.1%)
35 (57.4%) 26 (42.6%)
0.33 a
8 (57.1%) 6 (42.9%) 5 1
48 (78.7%) 13 (21.3%) 9 4
11 (78.6%) 2 (14.3%) 1 (7.1%)
55 (90.2%) 3 (4.9%) 3 (4.9%)
8 (57.1%) 6 (42.9%)
29 (47.5%) 32 (52.5%)
7 (50.0%) 5 (35.7%) 2 (14.3%)
35 18 2 6
0.17 a
0.52 a
(57.4%) (29.5%) (3.3%) (9.8%)
For statistical analysis: a Fisher’s exact test/Chi-square test, b Student’s t-test, c Mann–Whitney U-test.
reviewed the patients who underwent both conservative and operative treatments. Recent literatures demonstrated that the successful surgical repair was associated with pain relief.15,16,21 Therefore, the patients who underwent any kinds of brachial plexus surgery were excluded from our study. The characteristic of pain from previous literatures was described by several terms such as burning, crushing, and shooting or electric shock. Some patients even explained their symptom as \pin and needle" or \putting your fingers in a socket and somebody switching the socket on and off".13 However, the specific cause
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of pain was not defined by these studies. Finnerup et al.28 created a new tool named McGill Pain Questionnaire (MPQ) to assess the characteristic of pain. They revealed that the most common pain descriptors were shooting, penetrating, tingling, exhausting, and agonizing. It is believed that all brachial plexus injured patients would suffer from neuropathic pain which is the pain resulting from a primary lesion or dysfunction of the nervous system. However, Ciaramitaro et al.20 reported that only 67% of patients sustained brachial plexus injury experienced neuropathic pain. The remaining patients suffered from other kinds of pain termed as non-neuropathic pain. The clinical significance of neuropathic pain has been proposed in many literatures. Neuropathic pain is more chronic with stronger cognitive modulation than nociceptive pain. The response to specific classes of pain medications leads the physicians to get an accurate diagnosis between neuropathic or non-neuropathic pain. A new validated screening tool entitled Douleur Neuropathique en 4 questions (DN4) has also been developed and accepted as the standard tool for diagnosing neuropathic pain. The DN4 comprises seven items related to symptoms and three items related to clinical examination. The prevalence of neuropathic pain diagnosed by the DN4 varied from 67–95%.20,25 The sensitivity and specificity of the DN4 were 83% and 90% respectively compared to the clinical diagnosis of neuropathic pain.29 According to the DN4 questionnaire, Vanier et al.25 found that 95% of 60 brachial plexus injured patients suffered from neuropathic pain. Seventy five percent of these patients received the medical treatments, however, only 37% of the treated patients were satisfied with the outcomes of treatment. Ciaramitaro et al.20 evaluated 158 patients with traumatic peripheral nerve injury from four centres in Italy. Seventy-six patients had brachial plexus injury, which classified as brachial plexopathy in 54 patients and root avulsion injury in 22 patients. According to the DN4 questionnaire, the incidences of neuropathic pain in brachial plexus injured patients was 67%. Interestingly, all patients who had root avulsion injury suffered from neuropathic pain. Similar to our study, 97% of patients with brachial plexus injury experienced pain, and the incidence of neuropathic pain in these patients was as high as 76%. Eighty-five percent of neuropathic pain occurred within six weeks after injury, which was comparable to the previous study.18 The pathophysiology of neuropathic pain in brachial plexus injured patients was root avulsion and spinal cord
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deafferentation,11,17,20,30 non-avulsed root17,31 or cortical sensitisation.12,19,32 The treatment strategy ranged from empirical drug therapy, nerve transfer surgery and dorsal root entry zone (DREZ) surgery depending on severity of the pain.16,33,34 Medical treatment of neuropathic pain has recently been based on the recommendation of general practice guidelines developed from the majority of large randomized controlled trial including diabetes neuropathy and post herpetic neuralgia. The existing guidelines35,36 have not specified patients with brachial plexus injury and have a small body of evidence in treating neuropathic pain caused by brachial plexus injury.37 Medications, which have proved efficacy in treating different neuropathic pain conditions, may have the probability of being useful in additional conditions.38 However, it is possible that some neuropathic pain conditions may respond differently to the recommended treatment.39 By analyzing the medical treatment of neuropathic pain in our study, there were different analgesic treatment strategies from referring hospitals. The commonly prescribed medications were tricyclic antidepressant, gabapentin and tramadol, respectively. Similarly to previous literatures, medications given to our patients were the first line drugs of neuropathic pain treatment.18,25 Interestingly, more than half of the patients who had experienced pain did not receive any medications. These might probably be caused by lack of information, inexperience in severe disabling injury and underestimation of the pain. In a further evaluation of the intensity of pain between the treated and untreated group, the results demonstrated that there were no significant differences of VAS between both groups. Many factors may contribute to these outcomes including compliance, response to treatment, reassessment and dose adjustment. Factors related to neuropathic pain have been proposed in earlier literatures including severity and extent of injury. The significant correlation between pain intensity and the number of root avulsion was also demonstrated.18,21 In our study, there was significant correlation between types of brachial injury, classified as incomplete or compete injury according to numbers of root involvement, and the severity of neuropathic pain according to visual analogue scale. Root avulsion could be the major cause of the neuropathic pain. However, some authors proposed the conflicting data that non-avulsed roots had a possible role in pain generation.40 Diagnosis of root avulsion can be made by physical examination, cervical myelography, perioperative electrophysiology and direct intraoperative inspection of the exposed brachial plexus (if applicable).
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Myelographic findings were used to define the type of nerve root injury in our study. The results showed no correlation between myelographic findings and neuropathic pain. Environmental factors such as cold temperature and physical contact have been described as aggravating factors.39 In our study, we found no significant correlation between environmental factors and neuropathic pain. Because our study was carried out in the tertiary centre, where the severe injuries were predominant and might contribute to the selection bias, patients with neurapraxia that might improve without nerve surgery were not included.
CONCLUSION Hand Surg. 2015.20:39-45. Downloaded from www.worldscientific.com by FUDAN UNIVERSITY on 05/02/15. For personal use only.
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Neuropathic pain occurring in patients that have sustained a brachial plexus injury is commonly overlooked and underestimated, despite the 76% of incidence, resulting in reducing the overall outcomes even though the successful motor function recovery of the affected limb is possible. Clinicians should have high index of suspicion and must be careful in evaluating the neuropathic pain with both VAS and the screening tool (DN4) and treating this pain with the appropriate classes of pain medication to attain better quality of life in such patients.
ACKNOWLEDGEMENTS We would like to express our great appreciation to Dr. Pongparadee Chaudakshetrin for her valuable and constructive suggestions during the planning and development of this research work. Her willingness to give her time so generously has been very much appreciated. We would also like to extend our thanks to Narumol Sudjai for her help in offering us the statistical analysis of the results. All investigators have no conflict of interest.
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