Dorsal Root Entry Zone Lesioning for Brachial Plexus Avulsion Pain

CHAPTER 11

Dorsal Root Entry Zone Lesioning for Brachial Plexus Avulsion Pain CHRISTOPHER C. YOUNG, MBCHB, DPhil • ANDREW L. KO, MD

INTRODUCTION Brachial plexus avulsion (BPA) injuries occur in about 1% of polytrauma victims, predominantly in young males between 18 and 25 years of age, most commonly after motorcycle accidents (Fig. 11.1).1 Avulsion of the preganglionic dorsal nerve roots between the dorsal root ganglion and the spinal cord results in erratic firing of second-order sensory neurons in the dorsal horn and causes both paroxysmal and continuous pain.2 Both components may present immediately after trauma or months to years later and respond poorly to conventional treatments, including analgesics, antidepressants, and anticonvulsants. Neuromodulation via deep brain stimulation (DBS) and spinal cord stimulators has had statistically significant but unsatisfactory pain reduction, whereas ablative procedures such as medial thalamotomy, spinothalamic tractotomy, and anterolateral cordotomy have not demonstrated long-term benefits and are associated with disabling side effects.3 Microsurgical dorsal root entry zone (DREZ) lesioning, or DREZotomy, is a surgical procedure that has been used with success for the treatment of pain syndromes, spasticity, hyperactive bladder, and, in particular, chronic pain after BPA. The procedure consists of a microsurgical incision and bipolar coagulation of the lateral part of DREZ, the medial part of the tract of Lissauer, and extends to the apex of the dorsal horn.4 First performed by Sindou and colleagues in the 1970s, the purpose of DREZotomy is the selective destruction of nociceptive fibers grouped in the lateral bundle of the dorsal root, the excitatory fibers of medial tract of Lissauer, and the deafferented hyperactive neurons of the dorsal Rexed laminae (Fig. 11.3).2 Based on improved understanding of neuroanatomic pathways and neurophysiologic conduction of pain in the 1950s and 1960s, there was great interest

in anatomic lesioning for the treatment of pain.5 The gate control theory published in 1965 highlighted the possibility that the DREZ may be a suitable target for surgical lesioning for the treatment of chronic pain syndromes.6 The theory debunked the notion that pain is a simple transmission of nociceptive signals from peripheral receptors and the conduction of “pain” through the nervous system sensory apparatus. Instead, it hypothesized that pain is a patterned response that correlated to magnitude and pattern of sensory/nociceptive receptor stimulation. Peripheral stimulation evokes nerve impulses that are transmitted to the dorsal horn of the spinal cord and synapse with second-order sensory neurons of the ascending sensory pathway. The peripheral impulses are “gated” by a group of densely packed neurons known as the substantia gelatinosa (SG). SG has an inhibitory effect on the second-order afferents, and depending on the quality and magnitude of the peripheral nerve impulses, the SG regulates second-order afferent transmission via both positive and negative feedback loops and thus determines the nature of excitatory signal that is transmitted in the nociceptive spinothalamic pathway. In pathologic pain states, such as denervation hypersensitivity, the normal balance of peripheral nerve impulses arriving at the dorsal horn, i.e., SG, is disrupted and results in hyperactive firing of the deafferented second-order neurons.7 The DREZ is recognized as a complex network of neuronal connections, and disruption of this delicately balanced environment leads to abhorrent pain augmentation and transmission. DREZotomy thus involves the surgical destruction of erratically firing SG and second-order afferents to prevent the transmission of pain, analogous to the surgical resection of an epileptic cortical tissue to abolish seizure activity.3,8

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A

B

FIG. 11.1 T2-weighted magnetic resonance imaging (MRI) of the cervical spine in a patient involved in a high-speed motor vehicle collision. The patient sustained brachial plexus avulsion on the left with weakness in the C5-T1 myotomes. (A) The sagittal MRI shows evidence of ventral subdural blood product (large arrowheads). Additionally, there is elevation of the posterior longitudinal ligament along the posterior aspect of the dens. (B) The axial image shows displaced spinal cord with a ventral fluid collection concerning for a pseudomeningocele. The left aspect of the spinal cord at C7 is blunted with T2 signal abnormalities and the irregular nerve roots suggestive of nerve root avulsion (small arrowheads).

ANATOMY The DREZ is situated lateral to the midline in the dorsal spinal cord where cervical dorsal roots insert into the dorsal intermediolateral sulcus (Fig. 11.2). The normal DREZ is easily identified at the respective cervical level by the 6e11 rootlets that insert into the sulcus and can be found 2.2e3.5 mm lateral of the posterior median sulcus.9 The DREZ consists of three parts, including (1) the central grouping of dorsal rootlets, which enter the dorsal horn proximal to the pial ring within 1 mm of the dorsal intermediolateral sulcus, (2) the medial part of the tract of Lissauer, and (3) the Rexed laminae I-V of the dorsal horn, which include nucleus proprius and the SG where the afferent fibers synapse with second-order spinothalamic and spinoreticular afferents with input from the SG (Fig. 11.3). Microsurgically, DREZotomy targets the lateral grouping of central dorsal rootlets (small-diameter nociceptive fibers), the excitatory medial tract of Lissauer, as well as the nucleus proprius, the SG, and dorsal Rexed laminae, which contain deafferented hyperactive neurons.

PREOPERATIVE EVALUATION Before surgical intervention, patients must be thoroughly evaluated with regards to symptoms, etiology, treatments attempted thus far and response, and

appropriate diagnostic studies to ascertain whether the patients are suitable candidates for the procedure with a reasonable likelihood of deriving significant benefit from it. In the case of BPA injury, a careful history will reveal the mechanism of injury and the level of injury,

FIG. 11.2 Intraoperative photograph during DREZotomy. Note the normal nerve roots (triangles), which should be visualized above and below levels to be lesioned. This can be useful in locating the DREZ when anatomy is distorted by scarring. Also, note the pitting and scarring within the dorsal intermediolateral sulcus (arrows). An incision is being made at 45 degrees angle into the pia arachnoid of the spinal cord; this is continued in a staccato fashion along the length of the sulcus. Microbipolar cautery is used to complete the lesion through these openings in the pia arachnoid.

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Dorsal Root Entry Zone Lesioning for Brachial Plexus Avulsion Pain

DC

T

L

+ –

+

I II III +

ALP

IV-VII + IN MN

FIG. 11.3 Cross-sectional view of the cervical spinal cord

showing the DREZ and microsurgical anatomy of DREZotomy. The DREZ consists of three parts, including (1) the central grouping of dorsal rootlets, which enter the dorsal horn proximal to the pial ring within 1 mm of the intermediolateral sulcus, (2) the medial part of the tract of Lissauer, and (3) the Rexed laminae I-V of the dorsal horn, which include nucleus proprius and the SG where the afferent fibers synapse with secondorder spinothalamic and spinoreticular afferents with input from the SG. (Adopted from Sindou M. Microsurgical DREZotomy (MDT) for pain, spasticity, and hyperactive bladder: a 20-year experience. Acta Neurochir (Wien). 1995; 137(1e2):1e5; with permission.)

which can be confirmed on physical examination by focal neurological findings at the affected dermatome and myotome levels. Electrodiagnostic studies, such as nerve conductions, somatosensory-evoked potentials (SSEP), motor-evoked potentials (MEP) and electromyography, provide functional confirmation of injury. In BPA, somatosensory-evoked potential is obtained at the Erb’s point with absent cervical and cortical responses. Preganglionic BPA can be differentiated from postganglionic injuries by evaluating sensory nerve action potentials, which are disrupted by postganglionic lesions and preserved in BPA.10 Magnetic resonance imaging (MRI) of the brachial plexus and spine may provide additional information regarding localization of the injury, although up to 50% of

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patients with partial or complete root avulsion may have no observable meningeal alterations on MRI.4 However, we have shown recently that normal DREZ morphology on MRI may in fact be a positive predictive factor of a favorable response to DREZotomy in BPA pain.3 Furthermore, anatomical avulsion and sensory deficits do not always clinically correlate. In Sindou’s series, dorsal root avulsion seen at surgery and sensory deficits correlates only in 52% of patients. In 30% of patients, a larger sensory deficit is observed, whereas 14% of patients have a smaller deficit, and in 4%, the deficit is at an adjacent level. Nevertheless, there appears to be good correlation between the preganglionic root avulsion and pain territory and can be adequately treated by DREZotomy.11 Preganglionic root avulsion is much more likely to be associated with chronic pain compared with postganglionic root avulsion (82 vs. 33%), and the percentage of patients with chronic pain increases with the number of avulsed roots (71%, 82%, 85%, and 90% for two, three, four, and five avulsed roots, respectively) and approaching 100% for patients with total avulsion of all five levels.12

SURGICAL TECHNIQUE After endotracheal intubation, the patient is placed under general anesthesia. If using neurophysiological monitoring, total intravenous anesthesia is employed. Prophylactic antibiotics are administered. The patient is positioned prone on gel rolls, and a Mayfield head clamp is applied. For unilateral pathology, a midline incision is made, and a unilateral subperiosteal paraspinal muscle elevation is performed. Intraoperative fluoroscopy is used to confirm the correct spinal levels. Owing to the additional C8 cervical root and the topographic arrangement of the spinal segment in relation to the cervical vertebrae, the cervical spinal segment usually corresponds to the cervical lamina one level above; in other words, the C5-T1 nerve roots are found below the C4-C7 laminae. Hemilaminectomies are performed for operative exposure and are preferred for unilateral pathology as this technique allows the preservation of the spinous process and midline tension bands. Care is taken to avoid disruption of facet joint capsules to minimize mechanical sequelae from the procedure. Adequate exposure to allow visualization of the DREZ above and below the intended surgical target is essential as the normal anatomy at these levels often provide important reference for the localization of DREZ at the pathologic level which can be disrupted by scarring. The thecal sac is exposed by careful dissection of soft tissue. The operative microscope is brought in for durotomy and the remainder of the procedure.

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Under the operative microscope, durotomy is performed and the dural leaflets are retracted with holding sutures. Arachnoid adhesions, if present, may need to be freed. Microsurgical release of arachnoid tethering is important for correct anatomical localization of DREZ, and furthermore, it is postulated that arachnoid adhesions may cause meningeal irritation and contribute to pain symptoms. Pseudomeningoceles of the radicular dural sleeve are often encountered and can further distort the underlying spinal cord anatomy. The DREZ is carefully identified and inspected with reference to adjacent normal levels. In BPA, the affected DREZ may have pits, which mark the location of avulsed roots, or have a gray atrophic appearance. The dorsal intermediolateral sulcus is a critical anatomical landmark, which often contains a small radicular vessel within the sulcus. DREZotomies are made with staccato lesions using a sharp incision with a Beaver knife inserted ventromedially at 45 degrees angle into the intermediolateral sulcus to a depth of 2e3 mm (Figs. 11.2 and 11.4). This is followed by microbipolar cautery and targets the lateral dorsal rootlets, the medial portion of Lissauer’s tract, the nucleus proprius, and the SG in the dorsal horn. The lesions should span the intermediolateral sulcus from the normal rootlets above to those below the targeted level.

FIG. 11.4 Schematic depiction of DREZotomy viewed from

the dorsal spinal cord. Note the intermediolateral sulcus with avulsed cervical rootlets. Staccato lesions are created in the DREZ using microbipolar cautery. The target for lesion creation is the medal portion of Lissauer’s tract and the nucleus proprius to a depth of 2e3 mm. Entry into the cord at 45 degrees angle prevents damage to the adjacent lateral corticospinal tract.3

Surgeons have used variations of the above technique, with different types of microsurgical techniques, incorporating other modalities such as radiofrequency thermocoagulation,13 carbon dioxide laser,14 or ultrasound.15 Although direct comparisons of techniques have not been made, reported efficacy rates are similar without obvious advantages or disadvantages of one technique over the others. After the DREZotomy, the dura is closed primarily to prevent cerebrospinal fluid (CSF) egress, and the soft tissues are closed in standard fashion in layers. The presence of pseudomeningoceles at avulsed levels is important, as these can be the source of occult CSF leak; if found, care should be taken to primarily close any openings in the dura that are seen. Neurophysiologic monitoring with SSEP and MEPs is a useful adjunct in confirming spinal levels and providing an additional level of accuracy and safety. Intrafield stimulation can be used for the stimulation of ventral roots, if present, to confirm operative levels, as well as location of the midline if there is uncertainty regarding orientation of the spinal cord in the operative field.

POTENTIAL COMPLICATIONS As an invasive neurosurgical procedure, DREZotomy for BPA is for the most part a well-tolerated procedure. There are general surgical risks and potential complications associated with cervical spine surgery such as infection, CSF leakage, formation of pseudomeningoceles, and neural damage. Because of the traumatic etiology of BPA, the underlying anatomy may be abnormal and the presence of scar tissue may increase the risk of CSF leak and pseudomeningocele formation. Given the manipulation and lesioning of the cervical spinal cord, there is also the risk of permanent neurological damage, which includes motor weakness and sensory loss depending on the location of injury. For example, a lateral incision can damage the corticospinal tract with resultant ipsilateral hemiparesis. Similarly, the spinocerebellar tract may result in dysfunction of motor coordination. Damage to the posterior column in a lesion that is too medial can result in difficulties with balance and proprioception. A lesion that is too deep may sever sacral fibers and result in urinary dysfunction. In published series, motor weakness and sensory abnormalities are the most common complications. In Nashold’s and Ostdahl’s original series, 11 of the 21 patients (52%) had varying degree of persistent motor weakness, whereas 15 of the 21 patients experienced sensory changes after the procedure.8 More recent

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Dorsal Root Entry Zone Lesioning for Brachial Plexus Avulsion Pain

series reports significant lower rates of complication, and in one series 2 out of the 19 (11%) patients reported mild weakness at an average follow-up of 5 years.16 In a large single-center series followed for a mean of 6 years, neurologic complications were low, with 3 out of the 55 patients (5.4%) experiencing permanent disabling neurologic deficits, with 2 patients reporting disabling ipsilateral lower extremity weakness and a third patient with permanent genitourinary disturbances.4

OUTCOMES Efficacy and Durability of DREZotomy for BPA Pain Several single-center series have been published reporting outcomes after DREZotomy for BPA. Overall, DREZotomy provides significant and lasting alleviation of pain after BPA in approximately two-thirds of patients, and this has been replicated in a number of case series at centers around the world (Table 11.1). The single most important outcome measure in a treatment for pain is naturally the successful resolution of pain. However, successful treatment of pain or the definition of a “good” outcome is not always clear. A reasonable and commonly used definition is 50% improvement in pain with or without additional analgesics as measured on the visual analog scale. Using this criterion and analyzing published case series consisting of at least 10 patients followed for a minimum of 5 years, the reported rate of treatment success ranges from 54% to 90% (Table 11.1). In Sindou’s series consisting of 44 patients with a mean follow-up of 6 years, 65.9% of the patients experienced pain improvement by at least 50% with 71% reporting good quality of life.4 In our own experience, we reported a long-term success rate of 66% using the above criteria, which is commensurate with published results.3 Pain relief after DREZotomy for BPA appears to be lasting. The early series by Nashold and Ostadahl in the United States with a mean follow-up of 1.8 years reported very good or fair outcome in 55.6% and 16.7% of patients, respectively.8 When the follow-up times were extended and the results were reviewed a decade later in 1988, the rate of pain relief remained comparable with good outcome in 54% and fair outcome in 13% of patients.17 Sindou demonstrated excellent early outcome after the procedure with 94.6% of patients not requiring additional analgesic medication at the time of discharge from hospital after DREZotomy. This number dropped to 81.8% at 3 months follow-up, and at final follow-up at a mean

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of 6 years, 65.9% of patients experienced excellent or good outcome, with or without additional analgesics.4 Similarly, in a German series of 39 patients followed for a mean of 14 years, good pain reduction was achieved in 86% of the patients immediately postoperatively, 68% at 3 months, and 63% at 6 months, which remained stable at long-term follow-up, with an average pain reduction of 63% (SD 34%).18 In another series of 40 patients followed up for 10 years in Taiwan, rate of excellent or good pain control decreased from 80% early in the postoperative period to 60% at 5 year follow-up and 50% at 10 years.19

Prognostic Factors Several prognostic factors for successful pain relief after DREZotomy have been described, including the duration of pain, the characteristics of pain, and the presence of anatomic and imaging evidence of structural spinal cord abnormality (Table 11.2). A lengthier preoperative duration of pain has been correlated with better long-term results from DREZotomy. Interestingly, in one study, better results and sustained pain alleviation were obtained in patients with deafferentiation pain of more than 5 years at long-term follow-up, even though there was no difference noted postoperatively and at short-term (1 year) follow-up.20 In our own experience, the duration of pain before DREZotomy was significantly correlated with a better outcome, and all the patients in our study who had a poor pain outcome underwent DREZotomy within 36 months of the onset of deafferentiation pain.3 The duration of preoperative pain remained significant even after multivariable analysis with linear regression modeling. On the other hand, several other series did not find the duration of pain to be a significant prognostic factor.4,18 Clinical observations have suggested that different components of BPA pain may respond differently to DREZotomy and that it may have a more pronounced effect on paroxysmal pain. In a prospective case series, relief from paroxysmal pain is more likely than relief from constant pain after DREZotomy.21 There was a 11.5% statistically significant improved pain outcome in patients treated with paroxysmal pain compared with those treated with chronic pain. Similar favorable outcome for paroxysmal pain has been obtained for other destructive procedures treating pain of a spinal cord origin.22 Anatomic alterations to the spinal cord are common after BPA. Marked rotation or lateral deviation of the spinal cord was observed in a third to a half of patients, with associated gliosis and arachnoid adhesions.

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Review of Reported Case Series After DREZotomy3,4,16e18,20,21,26e28

Author

Country

Surgical Technique

Number of Patients

Collected Years

Mean Follow-up Years (Range)

Friedman et al. (1988)

USA

RF-Th

39

NA

5 (1e10)

Thomas and Kitchen (1994)

UK

RF-Th

44

10

Rath et al. (1996)

Germany

RF-Th

14

Samii et al. (2001)

Germany

RF-Th

Sindou et al. (2005)

France

MS

Prestor (2006)

Slovenia

Aichaoui et al. (2011)

PAIN RELIEF OUTCOME % OF PATIENTS Excellent

Good

COMPLICATIONS % OF PATIENTS

Fair

Poor

Motor

Sensory

54

13

33

40

40

5 (1e12)

68

11

21

22

18

16

6 (3e12)

57

14

29

43

NA

39

18

14 (2e18)

17

17

NA

44

15

6 (1e27)

34

32

34

1.8

3.6

MS

17

15

5

47

29

24

4

11

France

MS

26

10

5 (1e10)

23

3

7

Awad et al. (2013)

USA

RF-Th

13

25

5

37

32

NA

NA

Haninec et al. (2014)

Croatia

RF-Th

48

17

7 (2e14)

71

21

8

NA

NA

Ko et al. (2016)

USA

MS

27

18

8 (1e18)

34

0

0

63

31

77

66

16

16

These include series which contain at least 10 patients followed for more than 5 years. Pain reduction outcomes: Excellent ¼ 75%e100% pain reduction, Good ¼ 50%e75%, Fair ¼ <50%, Poor ¼ minimal effect. MS, microsurgery; NA, not available; RF-Th, radiofrequency thermocoagulation.

Functional Neurosurgery and Neuromodulation

TABLE 11.1

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Dorsal Root Entry Zone Lesioning for Brachial Plexus Avulsion Pain

TABLE 11.2

Prognostic Factors of Favorable Response to DREZotomy Longer duration of pain before surgery Paroxysmal pain Absence of spinal cord abnormality on MRI

Pseudomeningoceles are present in half of avulsed roots and are almost pathognomonic of BPA. Microscopically, focal gliosis and microcysts can be observed within the DREZ and dorsal horn in a third of cases, although the functional significance of these findings in relation to pain generation and response to DREZotomy is not well understood. MRI may have value in predicting immediate and long-term outcome after DREZotomy. Pain alleviation significantly and negatively correlated with the degree of abnormality seen on imaging of the spinal cord. An increase in the number of abnormalities (either intrinsic cord signal or DREZ avulsion) was correlated with a poorer outcome score. In a series of 27 patients followed for a mean of 8 years, all patients with MRI showing a normal spinal cord, without intrinsic signal abnormality or damage to the DREZ, had excellent or pain-free outcomes. In contrast, only 2 of the 12 patients with cord abnormalities on MRI had excellent relief from pain, and none were completely pain-free. One hypothesis to explain this phenomenon may be that if the success of DREZotomy is predicated based on the successful ablation of abnormally hyperactive interneurons within the DREZ, the extent of injury to the spinal cord may impact the success rate of this procedure. In other words, if the DREZ is injured to the point that the secondary nociceptive pathways are already inactive, then the procedure may be less successful. This may be because the pain is not the result of aberrant signaling within the spinal cord but the result of a more central process.

Other Treatment Modalities Spinal cord and DBS have been shown to provide pain relief after BPA. In Europe, DBS is approved for the treatment of neuropathic pain, and in a series of seven patients who underwent thalamic DBS for BPA pain, there was 52% reduction in pain at 1 year as measured by the visual analog scale.23 Spinal cord stimulators have also gained popularity because of the nonlesional and reversible nature of the procedure; however, its efficacy is thought to be lower when compared with

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DREZ.24 In a small series of 10 patients, different techniques for treating BPA pain were compared. Dorsal column stimulation and thalamic DBS were largely ineffective in comparison with DREZotomy.25 Other surgical ablative procedures such as medial thalamotomy, spinothalamic tractotomy, and anterolateral cordotomy have not demonstrated long-term benefits and have disabling side effects. Furthermore, within the existing literature that examines the efficacy of BPA treatment, there are no documented control groups when comparing outcomes. This is particularly relevant, given that the natural history of BPA pain is largely undetermined. One long-term study of patients with BPA who did not undergo surgical treatment reports that after 4 years, 25% of patients continued to have severe pain that was considered unacceptable and after 11 years this number dropped to 17%.11 However, within this cohort of patients, only 6% had spontaneous and complete remission of pain. It seems that the natural history of BPA pain is unremitting pain, but this becomes tolerable in a majority of patients; whether the rate of acceptable pain levels after surgical intervention is better than the rate of 75% after 4 years achieved by conservative observation is an open question.

CONCLUSION DREZotomy is a safe, effective, and durable treatment for pain resulting from BPA. Over the past 40 years, centers around the world have reported successful treatment of pain in two-thirds of patients undergoing the procedure. With refinement of microsurgical techniques and the availability of intraoperative neuromonitoring, success rates have improved and disabling complications are rare. Functional modalities such as spinal cord stimulation and thalamic DBS yield promise, and the nonlesional nature of these modalities are favored by many, although current results are inferior in comparison with DREZotomy.

REFERENCES 1. Midha R. Epidemiology of brachial plexus injuries in a multitrauma population. Neurosurgery. 1997;40(6): 1182e1188; discussion 1188e1189. 2. Sindou M. Microsurgical DREZotomy (MDT) for pain, spasticity, and hyperactive bladder: a 20-year experience. Acta Neurochir (Wien). 1995;137(1e2):1e5. 3. Ko AL, Ozpinar A, Raskin JS, Magill ST, Raslan AM, Burchiel KJ. Correlation of preoperative MRI with the long-term outcomes of dorsal root entry zone lesioning for brachial plexus avulsion pain. J Neurosurg. 2016; 124(5):1470e1478.

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4. Sindou MP, Blondet E, Emery E, Mertens P. Microsurgical lesioning in the dorsal root entry zone for pain due to brachial plexus avulsion: a prospective series of 55 patients. J Neurosurg. 2005;102(6):1018e1028. 5. Maccarty CS, Drake RL. Neurosurgical procedures for the control of pain. Proc Staff Meet Mayo Clin. 1956;31(7): 208e214. 6. Melzack R, Wall PD. Pain mechanisms: a new theory. Science. 1965;150(3699):971e979. 7. Loeser JD, Ward AA, White LE. Chronic deafferentation of human spinal cord neurons. J Neurosurg. 1968;29(1):48e50. 8. Nashold Jr BS, Ostdahl RH. Dorsal root entry zone lesions for pain relief. J Neurosurg. 1979;51(1):59e69. 9. Xiang J-P, Liu X-L, Xu Y-B, Wang J-Y, Hu J. Microsurgical anatomy of dorsal root entry zone of brachial plexus. Microsurgery. 2008;28(1):17e20. 10. Mansukhani KA. Electrodiagnosis in traumatic brachial plexus injury. Ann Indian Acad Neurol. 2013;16(1):19e25. 11. Parry CB. Pain in avulsion lesions of the brachial plexus. Pain. 1980;9(1):41e53. 12. Narakas A. Surgical treatment of traction injuries of the brachial plexus. Clin Orthop Relat Res. 1978;(133):71e90. 13. Rawlings 3rd CE, el-Naggar AO, Nashold Jr BS. The DREZ procedure: an update on technique. Br J Neurosurg. 1989; 3(6):633e642. 14. Young RF. Clinical experience with radiofrequency and laser DREZ lesions. J Neurosurg. 1990;72(5):715e720. 15. Dreval ON. Ultrasonic DREZ-operations for treatment of pain due to brachial plexus avulsion. Acta Neurochir (Wien). 1993;122(1e2):76e81. 16. Awad AJ, Forbes JA, Jermakowicz W, Eli IM, Blumenkopf B, Konrad P. Experience with 25 years of dorsal root entry zone lesioning at a single institution. Surg Neurol Int. 2013;4:64. 17. Friedman AH, Nashold BS, Bronec PR. Dorsal root entry zone lesions for the treatment of brachial plexus avulsion injuries: a follow-up study. Neurosurgery. 1988;22(2): 369e373. 18. Samii M, Bear-Henney S, Lüdemann W, Tatagiba M, Blömer U. Treatment of refractory pain after brachial plexus avulsion with dorsal root entry zone lesions. Neurosurgery. 2001;48(6):1269e1275; discussion 1275e1277.

19. Chen HJ, Tu YK. Long term follow-up results of dorsal root entry zone lesions for intractable pain after brachial plexus avulsion injuries. Acta Neurochir Suppl. 2006;99:73e75. 20. Prestor B. Microcoagulation of junctional dorsal root entry zone is effective treatment of brachial plexus avulsion pain: long-term follow-up study. Croat Med J. 2006; 47(2):271e278. 21. Aichaoui F, Mertens P, Sindou M. Dorsal root entry zone lesioning for pain after brachial plexus avulsion: results with special emphasis on differential effects on the paroxysmal versus the continuous components. A prospective study in a 29-patient consecutive series. Pain. 2011; 152(8):1923e1930. 22. Tasker RR, DeCarvalho GT, Dolan EJ. Intractable pain of spinal cord origin: clinical features and implications for surgery. J Neurosurg. 1992;77(3):373e378. 23. Pereira EAC, Boccard SG, Linhares P, et al. Thalamic deep brain stimulation for neuropathic pain after amputation or brachial plexus avulsion. Neurosurg Focus. 2013;35(3): E7. 24. Brill S, Aryeh IG. Neuromodulation in the management of pain from brachial plexus injury. Pain Physician. 2008; 11(1):81e85. 25. Teixeira MJ, De Souza EC, Yeng LT, Pereira WC. Lesion of the Lissauer tract and of the posterior horn of the gray substance of the spinal cord and the electrical stimulation of the central nervous system for the treatment of brachial plexus avulsion pain. Arq Neuropsiquiatr. 1999;57(1): 56e62. 26. Thomas DG, Kitchen ND. Long-term follow up of dorsal root entry zone lesions in brachial plexus avulsion. J Neurol Neurosurg Psychiatr. 1994;57(6):737e738. 27. Rath SA, Seitz K, Soliman N, Kahamba JF, Antoniadis G, Richter HP. DREZ coagulations for deafferentation pain related to spinal and peripheral nerve lesions: indication and results of 79 consecutive procedures. Stereotact Funct Neurosurg. 1997;68(1e4 Pt 1):161e167. 28. Haninec P, Kaiser R, Mencl L, Waldauf P. Usefulness of screening tools in the evaluation of long-term effectiveness of DREZ lesioning in the treatment of neuropathic pain after brachial plexus injury. BMC Neurol. 2014;14: 225.