Journal of Clinical Neuroscience xxx (2015) xxx–xxx

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Review

Deep brain stimulation for chronic pain Sandra G.J. Boccard ⇑, Erlick A.C. Pereira, Tipu Z. Aziz Oxford Functional Neurosurgery and Experimental Neurology Group, Nuffield Department of Clinical Neurosciences, University of Oxford, West Wing, Level 6, John Radcliffe Hospital, Headley Way, Oxford OX3 9DU, UK

a r t i c l e

i n f o

Article history: Received 7 April 2015 Accepted 11 April 2015 Available online xxxx Keywords: Anterior cingulate cortex Chronic pain Deep brain stimulation Periaqueductal grey Periventricular grey Sensory thalamus

a b s t r a c t Deep brain stimulation (DBS) is a neurosurgical intervention popularised in movement disorders such as Parkinson’s disease, and also reported to improve symptoms of epilepsy, Tourette’s syndrome, obsessive compulsive disorders and cluster headache. Since the 1950s, DBS has been used as a treatment to relieve intractable pain of several aetiologies including post stroke pain, phantom limb pain, facial pain and brachial plexus avulsion. Several patient series have shown benefits in stimulating various brain areas, including the sensory thalamus (ventral posterior lateral and medial), the periaqueductal and periventricular grey, or, more recently, the anterior cingulate cortex. However, this technique remains ‘‘off label’’ in the USA as it does not have Federal Drug Administration approval. Consequently, only a small number of surgeons report DBS for pain using current technology and techniques and few regions approve it. Randomised, blinded and controlled clinical trials that may use novel trial methodologies are desirable to evaluate the efficacy of DBS in patients who are refractory to other therapies. New imaging techniques, including tractography, may help optimise electrode placement and clinical outcome. Ó 2015 Elsevier Ltd. All rights reserved.

1. Introduction

2. Pain pathways

Pain was redefined in 1994 by the International Association for the Study of Pain as ‘‘An unpleasant sensory and emotional experience associated with actual or potential tissue damage, or described in terms of such damage’’ [1]. It is an experience with at least three dimensions: sensory (pain intensity), affective (pain unpleasantness) and cognitive. Neuropathic pain is a type of chronic pain in which symptom severity and duration are among the greatest [2]. Jensen and colleagues redefined it as a pain induced by a lesion or disease of the somatosensory system [3]. Chronic pain, with a prevalence of up to 8%, presents a huge burden on society costing at least $150 billion in the USA alone [4]. For patients with chronic pain, neurosurgery offers several types of treatments. In order to relieve intractable pain, several structures involved in the pain processing pathway have been targeted from the peripheral nerve through the dorsal root, spinal cord, midbrain, and thalamus to the cerebral cortex. Historically, these structures have been lesioned, perfused with analgaesics or anaesthetics and, of late, electrically stimulated. This review will focus on deep brain stimulation (DBS) for chronic pain treatment.

Pain comprises several components, therefore, its transmission pathways are complex. It is generally acknowledged that DBS can modulate activity in both lateral and medial pain systems [5]. The lateral one is composed of the spinothalamic tracts connecting the dorsal horn of the spinal cord to the ventral nuclei of the thalamus: the ventral posterior lateral (VPL), ventral posterior medial (VPM) and ventral posterior inferior nuclei. These tracts then project to the somatosensory cortices (primary and secondary). The medial pain system also consists of tracts connecting the spine to the thalamus (medial nuclei), but through the brain stem and connecting the limbic system. This second pathway is slower and is thought to modulate the affective component of pain [6].

⇑ Corresponding author. Tel.: +44 1865 231845. E-mail address: [email protected] (S.G.J. Boccard).

3. DBS DBS is widely used in movement disorders. Its efficacy has also been demonstrated in epilepsy, Tourette’s syndrome, obsessive compulsive disorders and cluster headache [7]. The concept of relieving intractable pain with DBS appeared in the 1950s, a decade before the gate control theory. The first evidence arose from rodent models. In self-stimulation experiments, rats with implanted electrodes robustly sought stimulation of the septal region that resulted in a feeling that Olds et al. interpreted as a form of pleasure [8]. Subsequently, Heath

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S.G.J. Boccard et al. / Journal of Clinical Neuroscience xxx (2015) xxx–xxx

hypothesised that, as pain is the opposite of pleasure, stimulation of the septal area could provide pain relief. One of his patients who was suffering from cancer pain reported analgaesia after receiving septal DBS [9]. Later on, other terminal cancer pain patients were also relieved by septal area DBS [10]. At the end of the 1970s, DBS for pain was acknowledged as safe and effective by practitioners in the field [11], and the USA Food and Drug Administration (FDA) asked the three DBS systems manufacturers of the time to conduct studies to demonstrate its benefit. Only one company complied and it provided data that demonstrated only limited efficacy. Consequently, the approved status of DBS for pain was rescinded and it is still ‘‘off label’’, preventing funding approval by insurers [12,13]. Therefore, only a small number of neurosurgeons offer DBS for pain [14]. Moreover, without clear indications, randomised controlled trials and long term follow-up, DBS for chronic pain may not be established. In Europe, DBS for chronic pain has been approved by the European Federation of Neurological Societies and the United Kingdom National Institute for Health and Clinical Excellence [14,15]. Worldwide, an increasing interest in DBS for chronic pain refractory to medical treatment has been observed with the publication of an increasing number of papers over time (Fig. 1). Among them, several studies, mainly open labelled, have reported its efficacy in various aetiologies including phantom limb pain [16–20], brachial plexus injury [19–22], central post-stroke pain [17–19,21–23], face pain [17,19,24,25], spinal injuries or failed back surgery syndrome [17–19,22] and headaches [25–29] (Table 1). 4. DBS targets Historically, many brain areas have been targeted, starting with the septal region [9,10], the sensory thalamus (both lateral [VPL] or medial [VPM] nuclei) [16–19,21,24,31,54,61,65,73,74], the periventricular grey (PVG) and periaqueductal grey (PAG) [17– 19,23,41,61,65,74], the internal capsule [65,74], the posterior hypothalamus [25–29], the nucleus accumbens [23] and, finally, the anterior cingulate cortex (ACC) [22,75]. The choice of the targeted area depends on the type of pain and its distribution. 4.1. The sensory nuclei of the thalamus (VPL, VPM) With regards to the VPL and VPM, insights came from ablative surgery [76]. As reported in large case series of DBS for chronic

pain, sensory thalamic stimulation has been used with varying effectiveness in several chronic pain syndromes [19,20] with the VPM particularly targeted in facial pain [24]. Thalamic targets are 10–13 mm posterior to the midcommissural point. Depending on the pain site, the best location can be from 5 mm inferior to 2 mm superior to it. The VPM, targeted for face pain only, is found between the wall of the third ventricle and the internal capsule. The VPL is targeted 2–3 mm medial to the internal capsule for the arm pain, and 1–2 mm for the leg area. The stimulation induces a pleasant paraesthesia in the painful area. 4.2. Periventricular grey/periaqueductal grey Initially, the PVG and PAG were identified as targets for DBS in animal research. Rodent experiments demonstrated PVG and PAG grey regions as DBS targets [77]. These findings were subsequently translated to humans [24,41] and widely used by several functional neurosurgeons. The PVG is surrounded by the medial lemniscus laterally, superior colliculus posteriorly and the red nucleus anteriorly. The electrode is placed 2–3 mm lateral to the third ventricle at the level of the posterior commissure. When these areas are stimulated, the pain is substituted by a sensation of warmth or analgaesia. Stimulation of the PVG also induces some changes of autonomic functions [78–81]. Electrode location in the PAG and the sensory thalamus can be seen in Figure 2. 4.3. Anterior cingulate cortex While somatosensory homunculi have been demonstrated in the ventral posterior thalamus [82] and later in the PAG/PVG [83], outcomes of DBS of these targets appear less good for whole or hemi-body pain. Hemi-or whole-body post-stroke pain may benefit from targeting of regions involved in the affective dimension of chronic pain such as the ACC [84]. Changes in activity of the ACC have been shown to induce effects on many psychological and motor functions [85,86], and have also been demonstrated to be involved in empathy and pain expectation [87]. Historically, cingulotomy has been used to relieve intractable pain, in particular in terminal cancer. Freehand resective cingulectomy was first performed in Oxford by Cairns [88], and stereotactic cingulotomy later in Massachusetts by Ballantyne [89]. A review of published cingulotomy series showed that the procedure was useful in 32–83% of patients, depending on the study [90]. Interestingly, many positron

Fig. 1. Graph of the number of papers on deep brain stimulation (DBS) for chronic pain in humans (reviews excluded). The main source of articles for this review was PubMed with the following search terms: ‘‘stimulation’’ + ‘‘pain’’ + ’’patients’’; March 2015. Excluded were studies performed on animals, or those that were not specifically on chronic pain or DBS.

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S.G.J. Boccard et al. / Journal of Clinical Neuroscience xxx (2015) xxx–xxx Table 1 Summary of published case series on deep brain stimulation for chronic pain Authors

Reference Study label

Patients, Aetiology n

Target

Stimulation

Follow-up

Success,%

Heath Gol Mazars et al.

[9] [10] [30–33]

Open Open Open Open [24,34,35] Open

1 6 84 121 5

Cancer pain Terminal carcinomatosis Chronic pain syndromes Chronic pain syndromes Facial anaesthesia dolorosa

Septal region Septal region PAG/PVG VP VPM

NA NA NA

NA NA NA

NA

NA

100 17 0 69 80

[36]

122

Chronic pain syndromes

PAG (n = 65)

200–300 ls; 20–30 Hz; 2–4 V 200–300 ls; 50–100 Hz; 2–6 V NA Self-stimulation NA

2–14 years

77

Hosobuchi, Adams et al.

Open

VP (n = 76) [37–39] Richardson and Akil [40–44] Thoden and [45] Dieckmann [46] Mundinger and [47] Salomão Gybels [48–50]

Open Open Open

NA 30 26

Chronic pain syndromes Chronic pain syndromes Chronic pain syndromes

IC PAG/PVG PAG/PVG

Open Open

20 32

Chronic pain syndromes Central pain

7 36 6 19 28 14

Chronic pain syndromes Chronic pain syndromes Chronic pain syndromes Neurogenic pain Chronic pain syndromes Spinal cord pain (n = 9) Midbrain injury (n = 1) Phantom limb pain (n = 1) Median nerve causalgia (n = 1) BPI (n = 1) Supraorbital causalgia (n = 1) Chronic pain syndromes Chronic pain syndromes Chronic pain syndromes Chronic pain syndromes

NA NA 6–54 months

NA 66 28

VP NA Leminiscus medialis NA

47 months

53

PAG/PVG VP PAG/PVG Septum pf-CM VP

NA NA NA NA NA 75–100 Hz

NA 48 months 6–42 months 1–10 years A few months 10 months

16 30 33 63 76 72

PAG/PVG VP VP PVG

NA

3 years

79

NA NA

NA 6 months to 4 years

63 77

NA

6 months to 10 years

63

Schvarcz

[51,52]

Open Open Open

Ray and Burton Turnbull et al.

[53] [54]

Open Open

Plotkin

[55]

Open

Tsubokawa et al Kumar et al.

[56–58] [59]

Open Open

48 12 24 18

[60]

Open

48

Chronic pain syndromes

VP PVG

[61]

Open

68

Chronic pain syndromes

VP PVG (n = 49) VP (n = 20)

Young et al.

[62,63]

Open

48

Levy et al.

[64] [65]

Open Open

17 141

Siegfried Tasker et al.

[66] [67]

Open Open

89 25

FBSS (n = 16) Cancer (n = 7) Spinal cord injury (n = 6) Postoperative pain (n = 4) Anaesthesia dolorosa (n = 4) BPI (n = 4) Post traumatic pain (n = 4) Post herpetique neuralgia (n = 2) Glossodynia (n = 1) Cancer pain Nociceptive (n = 57) Deafferentation (n = 84) Chronic pain syndromes Chronic pain syndromes

Coffey, RJ

[68]

196

Pain

Aziz et al.

[19,69– 72]

Multicenter trial Open

PAG/PVG PAG/PVG (n = 57) VP (n = 84) VP PAG/PVG VP NA

85

Phantom limb (n = 9)

PAG/PVG VP

[20]

Open

12

Brachial plexus injury (n = 7) Post stroke pain (n = 31) Spinal pathology (n = 13) Head and facial pain (n = 15) Other pains (n = 10) Phantom limb (n = 5)

[22]

Open

16

Brachial plexus injury (n = 7) Brachial plexus injury (n = 3)

58

PAG/PVG VP IC

100–500 ls; 25–50 Hz; 78 months 1–5 V 200–800 ls; 50–100 Hz; 2–8 V NA 20 months

62

NA NA

1–21 months 80 months

NA NA

50) [18,19,61]. Furthermore, even in the large series, loss of follow-up limits the power of analysis. Finally, a large heterogeneity in DBS efficacy is observed. This disparity may be due to differences in study design and pain assessment tests, or indeed individual differences between patients. Of course, there are several other neurosurgical options to treat refractory pain syndromes. Motor cortex stimulation is one that also acts directly upon the brain [130]. It can also relieve pain in approximately two thirds of patients suffering from intractable chronic pain, but there is little evidence that it is more effective than DBS [129]. In our hands, DBS has been more effective than motor cortex stimulation for several pain syndromes [69]. The observed differences in efficacy between groups may be explained by varying surgeon expertise in particular techniques. Finally, even when DBS is truly efficacious, tolerance may manifest after several years. This may be overcome by slight changes in stimulation settings or by interrupting the stimulation periodically. Technological advances such as so-called smart adaptive stimulation may allow patients to better control pain and reduce tolerance. In conclusion, DBS for pain has been shown to be effective in several patient series. However, clinical trials are required to more robustly demonstrate the efficacy of DBS to treat intractable chronic pain and regain FDA approval. The nature of the trial design may not necessarily require large numbers of patients for randomised controlled trials [131] in particular because DBS can be switched on and off and patients blinded to its settings. Conflicts of Interest/Disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication.

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Acknowledgements The authors are supported by the National Institute for Health Research (NIHR) Oxford Biomedical Research Centre based at Oxford University Hospitals National Health Service Trust and the University of Oxford. The views expressed are those of the authors and not necessarily those of the NHS, the NIHR or the Department of Health. The authors have no personal, financial or institutional interest in any of the drugs, materials, or devices described in this article.

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Please cite this article in press as: Boccard SGJ et al. Deep brain stimulation for chronic pain. J Clin Neurosci (2015), http://dx.doi.org/10.1016/ j.jocn.2015.04.005

Deep brain stimulation for chronic pain.

Deep brain stimulation (DBS) is a neurosurgical intervention popularised in movement disorders such as Parkinson's disease, and also reported to impro...
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