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Motor cortex stimulation for central pain following a traumatic brain injury
Pain 123 (2006) 210–216 www.elsevier.com/locate/pain
Case report
Motor cortex stimulation for central pain following a traumatic brain injury Byung Chul Son b
a,*
, Sang Won Lee a, Eun Seok Choi b, Jae Hoon Sung a, Jae Taek Hong
a
a Department of Neurosurgery, St. Vincent’s Hospital, The Catholic University of Korea, Suwon, Republic of Korea Department of Rehabilitation, Daejeon St. Mary’s Hospital, The Catholic University of Korea, Daejeon, Republic of Korea
Received 5 August 2005; received in revised form 18 January 2006; accepted 21 February 2006
Abstract Central pain can occur in any lesions along the central nervous system affecting the spinothalamocortical pathway. Although diverse etiologies have been reported to cause central pain, there are few reports on the occurrence and surgical treatment of central pain following a traumatic brain injury (TBI). This paper describes the occurrence of central pain following a severe TBI, in which the diagnosis of central pain was typically delayed due to the patient’s decreased ability to express his pain for severe aphasia as a neurological sequela. The severe burning pain, deep pressure-like pain, and deep mechanical allodynia, which presented over the contralateral side to the TBI, were successfully relieved with motor cortex stimulation (MCS). The analgesic effect of stimulation was found to be long lasting and was still present at the 12-month follow up. As shown in this patient, the occurrence of central pain syndrome should be considered by physicians caring for TBI patients, and a comprehensive, systematic study will be needed to determine the prevalence of central pain after a TBI. Ó 2006 International Association for the Study of Pain. Published by Elsevier B.V. All rights reserved. Keywords: Central pain; Traumatic brain injury; Motor cortex stimulation
1. Introduction In 1994, central pain was defined by the International Association for the Study of Pain as ‘‘pain initiated or caused by a primary lesion or a dysfunction within the CNS’’ (Merskey and Bogduk, 1994). The reported causes of central pain are vascular lesions in the brain and spinal cord, multiple sclerosis, traumatic spinal cord injury, traumatic brain injury, syringomyelia and syringobulbia, tumors, abscesses, viral and syphilitic myelitis, epilepsy, and Parkinson’s disease. In addition to central pain caused by spontaneous lesions, surgical lesions of the central nervous system such as cordotomy also cause central pain. The highest prevalence of central pain has been observed to be a result of lesions in the spinal cord, *
Corresponding author. Tel.: +82 031 249 8202; fax: +82 031 245 5208. E-mail address: [email protected] (B.C. Son).
lower brainstem, and ventroposterior part of the thalamus (Bonica, 1991; Boivie, 1992; Tsubokawa and Katayama, 1998). Considering that traumatic brain injury (TBI) is a common cause of neurological morbidity around the world, and the spinal cord is a known lesion location, where the highest prevalence of central pain occurs, it is surprising that there are very few reports on the occurrence of central pain after a TBI (Boivie, 1999). There has been no clear explanation for this discrepancy of occurrence of central pain between brain and the spinal cord. Motor cortex stimulation (MCS) was first proposed for the treatment of central pain and has been shown to be effective in relieving peripheral neuropathic pain (e.g., trigeminal neuropathic pain, brachial plexus avulsion, and phantom pain) (Myerson et al., 1993; Tsubokawa et al., 1993; Nguyen et al., 1997; Tsubokawa and Katayama, 1998; Saitoh et al., 2000). According to
0304-3959/$32.00 Ó 2006 International Association for the Study of Pain. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.pain.2006.02.028
B.C. Son et al. / Pain 123 (2006) 210–216
a review of the literature, Nguyen et al. (1997) reported the result of MCS in one patient with central pain following a brain injury in 1997. However, the long-term results at 12 months were unsuccessful and the details were not reported. Because the report of central pain following a TBI is extremely rare, and medically intractable central pain conditions are notoriously resistant to treatment, we report a patient whose intractable central pain following TBI was successfully alleviated with MCS. 2. Case report 2.1. History and examination A 43-year-old right-handed man presented with a severe spontaneous burning pain in his right hand, forearm and right lower leg and foot, in addition to heaviness and deep pressure-like pain in his right lower leg including the foot. Two and a half years prior to admission, he fell from an electricity pole and sustained a severe TBI. Initially, he was comatose as a result of an acute subdural hematoma in his left convexity with multiple intracerebral contusions in his left temporal and frontoparietal lobe, he underwent an emergency decompressive craniectomy and an evacuation of the subdural hematoma and intracerebral hemorrhagic contusion. He was semicomatose after surgery and regained consciousness over a 1-month period after the injury. However, severe motor aphasia and a dense hemiplegia associated with a hemisensory deficit developed. During the subsequent 6 months, he was taken to the rehabilitation unit. His weakness progressively improved with active physical therapy, and finally he could stand and walk with assistance. Approximately 1 year after the accident, he could walk by himself slowly with a cane and a short leg prosthesis. However, he was hesitant to perform active exercise and finally refused to visit the rehabilitation unit. His wife who had been caring for him finally disclosed that he was suffering from a burning sensation and heaviness in his right lower leg and his arm. Indeed, he felt a gradually developing burning sensation in his right foot 6 months after the injury, which ascended slowly to the right upper leg, to the right inguinal area during the following 6 months, and deep pressure-like pain, heaviness, and crushing developed in his right leg. Approximately, one year after the accident he began to feel a burning pain in his right hand, which has ascended to his right forearm, and another area of burning developed in his right lower back. He also felt a deep pressure sensation in his right shoulder, which was regarded as a type of musculoskeletal pain associated with a frozen shoulder. Because of the progressive difficulty in performing exercise and his withdrawal response, he underwent a careful interview and sensory
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examination. As a result, he was finally diagnosed with a central pain following a TBI approximately 18 months after the accident and 1 year after the development of pain. After the central pain had been diagnosed, the maximum medical treatment was provided for 3 months but, his pain progressively worsened. The burning sensation in his leg and arm was constant, and he experienced an intermittent cramping pain. His pain was aggravated as a result of exposure to cold temperatures, humidity, and emotional upsets. During the 2 months prior to referral, he could barely sleep at night, stroking his right leg and right hand due to the severe heaviness and burning. His pain medication regimen at the time of referral was as follows: gabapentin 2400 mg, paroxetine 20 mg, tramadol 200 mg, trazodon 25 mg, oxycarbamazepine 600 mg, and amitryptyline 30 mg a day. At the time of referral, his VAS was 75–85/100. A physical examination showed that he had residual motor weakness (grade 4/4) which was more severe in the distal arm and leg. He showed a hemiplegic gait and moderate rigidity in his arm and leg, he could walk by himself slowly and carefully in a guarded fashion. Hypesthesia to light touches in addition to pinprick hypoalgesia, which was more severe in the painful areas, was present on his right hemibody including face. In his right arm and leg, i.e., the painful areas, there was decreased thermal sensation, particularly cold. There was a severe mechanical deep pressure allodynia in his right leg and foot. However, no spontaneous paresthesia and other types of mechanical allodynia, such as static, dynamic, and cold allodynia were found. Fig. 1 shows the distribution of his pain and sensory deficits. His mentality was clear without confusion and disorientation. However, severe motor aphasia with stuttering was noticed and his speech was difficult to understand. He had difficulty in naming and showed some shortterm memory impairment. The magnetic resonance imaging showed extensive damage to the left frontal, temporal, insular, and parietal lobe (Fig. 2). Severe encephalomalacic changes to the posterior part of inferior frontal gyrus, were thought to be the cause of motor aphasia. 2.2. Surgical procedure An anatomical localization of the central sulcus was performed using a three-dimensional image-guided navigation system. After marking the course of the central sulcus over the left convexity and the vertex, an approximately 10-cm-long linear incision was carried out, and an approximately 7-cm-diameter craniotomy was performed under general anesthesia. The surgical procedure performed in this patient was similar to those reported previously (Nguyen et al., 1997; Katayama et al., 1998; Tsubokawa and Katayama, 1998; Son et al., 2003).
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as a ‘hand knob’ (Yousry et al., 1997), and this electrode was placed subdurally along the mediolateral somatotopy of the precentral gyrus because the overlying dura mater was thickened as a result of previous trauma surgery. Another electrode for stimulating the lower leg was placed epidurally, parallel to the course of the superior sagittal sinus, as recommended elsewhere (Fig. 3) (Katayama et al., 1998; Tsubokawa and Katayama, 1998). During the 7-day test stimulation period, significant pain relief was observed when a 21 Hz, 210 ms, 0.8–1.2 V (‘‘0’’ negative, ‘‘3’’ positive, continuous mode) for the forearm electrode and 30 Hz, 210 ms, 2.0–2.5 V (‘‘0’’ negative, ‘‘2’’ positive, continuous mode) for the leg and foot stimulation combinations were used. During stimulation, a warm, vibrating paresthesia was produced in his right hand, forearm, right lower trunk, and his lower leg including the foot. Two pulse generators (Itrel IIIÒ, model 7425, Medtronic Inc., Minneapolis, MN) were implanted in each side of the upper chest after the induction of anesthesia (Fig. 3). 2.3. Results of pain relief
Fig. 1. Schematic diagram showing the distribution of central pain after a TBI. The horizontally hatched areas indicate severe spontaneous burning pain. The obliquely hatched area shows heaviness and pressure-like squeezing pain. Hypesthesia and hypoalgesia to a pinprick were noted in the right side of the body including face.
We were unable to obtain an adequate motor contraction with direct cortical stimulation up to 18 mA used to identify the neurophysiological somatotopy of the precentral gyrus despite the discontinuation of the muscle relaxant well before beginning the direct precentral gyrus stimulation with a bipolar cortical stimulator. Therefore, the location of the stimulating electrode (Resume IIÒ, model 3587A, Medtronic Inc., Minneapolis, MN) for the hand and forearm was determined according to the anatomical imaging landmark indicating a motor hand area that was previously described
The level of stimulation was adjusted until satisfactory pain relief had been achieved by setting the electrodes at 21–30 Hz, 210 ms, and 0.8–2.4 V. The post-stimulation analgesic effect was estimated to last approximately 5 min, and a continuous mode of stimulation was delivered. Visual analogue scales, which were graduated from 0 to 100, were used to assess the extent of pain relief. However, the McGill Pain Questionnaire could not be assessed in this patient due to severe aphasia (Melzack, 1975). The effect of stimulation was evaluated preoperatively and 12 months post-operatively. The visual analogue scale score improved 75–85 to 20–30 with stimulation, and the spontaneous burning pain in the right forearm, hand, and lower trunk improved by 90–95%. The burning pain, heaviness, and deep pressure-like pain in his right leg improved by 70–80%. However, the heaviness and deep pressure allodynia in his foot improved by only 50%. The patient’s pain changed minimally over the 12 months of follow up. The shoulder pain previously believed to be a type of musculoskeletal pain also improved and the range of motion in his right shoulder increased much more with the alleviation of pain, he could elevate his shoulder again. An unwanted motor contraction and seizure activity was not been observed. After 12 months of stimulation, the patient’s medication was decreased to 900 mg gabapentin and 10 mg amitriptyline per day. 3. Discussion Although head trauma had been reported to be a cause of central pain, there are few reports on the
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Fig. 2. Radiological findings showing the anatomical location of central pain following a TBI. (A) T1-weighted magnetic resonance image shows that extensive damage to the insular cortex and perisylvian temporoparietal opercular areas. Note the severe loss of the insular cortex and the underlying white matter, which interferes with the thalamocortical transfer of nociceptive information. (B) T1-weighted magnetic resonance image demonstrates additional damage to the post-central gyrus and white matter in the parietal lobe.
occurrence of central pain after a TBI (Berthier et al., 1988; Boivie, 1999; Yezierski, 2002). Until now, it is uncertain why TBI causes central pain so rarely.
Fig. 3. Post-operative skull X-ray image showing the placement of the two laminotomy electrodes in the left hemisphere. There are two previous craniotomy sites on each side of the calvarium and a new craniotomy for the placement of an electrode for motor cortex stimulation.
However, it is possible that central pain itself is often overlooked as a possibility in patients with a CNS disease because of a lack of knowledge of its characteristics (Boivie, 1999). This may cause puzzling symptoms when several coexisting pains of an unusual nature exist. One reason for the lack of knowledge of central pain is the fact that relatively little systematic research has been carried out on the clinical aspects of central pain. In addition, the lack of experimental models for central pain until recently hampered research into its mechanisms (Boivie, 1999). Burning pain and deep pressure-like pain in this patient localized within the region of hypoesthesia and he showed severe deficits in his ability to detect pain and cold, as well as clear deficits in touch and proprioception. Thus, this patient with central pain due to TBI showed a clinical picture similar to CPSP. CPSP patients generally have clear somatosensory deficits and a paradoxical ongoing spontaneous pain that is felt within the area of deficit. Central pain can be experienced as superficial or deep pain, or both superficial and deep components, but the high incidence of cutaneous hyperesthesias contributes to the impression that superficial pain dominates, although deep pain is common too. In this particular patient, only mechanical deep pressure allodynia was noted. In CPSP, cutaneous hyperalgesia, allodynia, and/or hyperpathia are frequently, but not invariably, present (Boivie and Leijon, 1991; Boivie, 1999). Recently, dissociation between cutaneous and deep sensibility in CPSP has been reported (Mailis and Bennett, 2002). Several areas of the brain, fronto-temporal and insular, and parietal lobes in this patient were severely damaged (Fig. 2). Among them, the areas particularly
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related to the pathophysiology of central pain are the insular and parietal lobes. The parietal or insular regions have been shown to be associated with central pain (Michel et al., 1990; Schmahmann and Leifer, 1992; Boivie, 1999). Schmahmann and Leifer (1992) studied the anatomic correlations in 6 patients with central pain as a result of lesions of the parietal lobe, and reported that the common area of involvement in their cases was the white matter deep to both the caudal insula and the opercular region of the posterior parietal cortex. They suggested that a disruption of the interconnections between these cerebral cortical areas (including the second somatosensory representation, SII) and the thalamus, particularly the intralaminar and ventroposterior nuclei, might be responsible for the occurrence of central pain syndrome namely, parietal pseudothalamic pain syndrome. The extensive area of damage to the insula in this patient was consistent with those reported by Schmahmann and Leifer (1992). The middle/posterior insular cortex is known to be the area where discriminative thermosensory sensation is represented in humans (Craig et al., 2000). The functional anatomy in monkeys indicates that a dedicated thalamic nucleus relays the topographic, discriminative thermoreceptive-specific, and nociceptive-specific lamina I spino- and trigeminospecific projections to the dorsal margin of the middle/posterior insular cortex (Craig et al., 1994, 1999). Data from a PET imaging study of a thermal grill illusion of pain and an fMRI study indicate that a strong innocuous cool stimulation (20 °C) activates the contralateral insular cortex, but not the parietal cortex (Craig et al., 1996; Davis et al., 1999). These findings support the proposal that central pain results from loss of the normal inhibition of pain by cold (Craig et al., 1994, 2000), because the lesions involving the insula can produce central pain (Schmahmann and Leifer, 1992). The parietal opercular area including the SII was also damaged in our patient (Fig. 2B). Lesions of the SII and the insula produce asymbolia for pain, suggesting that the SII is an important cortical locus for the conscious perception of noxious stimuli (Biemond, 1956; Mesulam and Mufson, 1985; Berthier et al., 1988). The anatomical and electrophysiological data show that in monkeys, these regions receive direct nociceptive input (Ploner et al., 1999; Craig et al., 2000). Experimental and lesion data in humans suggest these areas are associated with the motivational-affective aspects of pain and the sensory-discriminative components of pain perception (Vogt et al., 1993; Craig et al., 1996; Rainville et al., 1997; Ploner et al., 1999). Although MCS has been proven to be a promising treatment for various central and peripheral neuropathic pain, the precise analgesic mechanism of MCS is still unclear (Garcı´a-Larrea et al., 1997; Nguyen et al., 1997; Katayama et al., 1998). Tsubokawa and Katayama
have suggested that MCS might produce an analgesic effect through the orthodromic and/or antidromic activation of the fourth-order antinociceptive neurons, which secondarily results in the inhibition of hyperactive nociceptive cortical neurons, that restores the inhibitory surrounding field around the restricted area of excited neurons in the somatosensory cortex (Tsubokawa et al., 1993). However, MCS has not been shown to produce any significant cerebral blood flow (CBF) changes in the parietal cortex, suggesting that the sensory cortex is not the key structure (Peyron et al., 1995; Garcı´a-Larrea et al., 1999; Nguyen et al., 1999). On the other hand, positron emission tomography (PET) studies suggest that the thalamus is an important structure in the mediation of the functional MCS effects, and MCS exerts its analgesic effect by modulating the thalamic activity (Nguyen et al., 1999; Son et al., 2003; Saitoh et al., 2004). Studies on groups of patients with intractable pain with various origins have confirmed the existence of significant CBF increases during MCS in the lateral and medial thalamus, anterior cingulate-orbitofrontal cortex (BA32), the anterior insula-medial temporal lobe, and the upper brainstem (Garcı´a-Larrea et al., 1997). The thalamic area showing the most significant CBF changes are the ventrolateral and ventroanterior nuclei, i.e., the thalamic regions directly connected to the motor and premotor cortices. However, these clinical and PET studies could not explain how MCS relieves the CPSP, which has a damaged thalamus, where the substrate for the functioning MCS has already been destroyed by the stroke. Recently, Saitoh et al. (2004) showed in a patient with CPSP that was caused by a thalamic hemorrhage that a successful MCS induced a significant CBF increase in the contralateral hemisphere (thalamus, gyrus rectus, and superior frontal cortex) compared with the stimulated one, suggesting that the efficacy of MCS was mainly related to the increased synaptic activity in the thalamus. As an explanation for the contralateral thalamic activation, they suggested that the reorganization of the major thalamic function to the contralateral side and the contralateral thalamus in the dominant hemisphere might play a more important role in their particular patient. It has already been reported that right post-stroke pain disappeared after an additional contralateral left parietal lobe lesion (Helmchen et al., 2002). It is now known that only approximately 1/2 of the pyramidal tract fibers, which are those constituting the corticospinal tract itself, actually terminate in the spinal cord (Wisendanger, 1969; Davidoff, 1990). Many pyramidal tract axons terminate in, or send collateral branches to, a number of supraspinal structures that are generally considered to be sensory in function (e.g., sensory and motor nuclei of the thalamus, trigeminal
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nucleus, dorsal column nuclei, striatum, red nucleus, pontine nuclei, midbrain and bulbar reticular formation, and inferior olive) (Wisendanger, 1969; Armand, 1982). Indeed, physiological studies indicate that the pyramidal tract contains many fibers of a cortical origin that affect the sensory input and somatosensory transmission at each synaptic relay at both spinal and subcortical levels. The pyramidal tract can be regarded as an internuncial pathway intercalated between the subcortical structures, the cortical structures, and the afferent inputs from the peripheral sensory receptors and spinal motoneurons, and provides a pathway for the corticofugal regulation of various sensory relays. This control of the sensory inflow into the central structures can influence the type and amount of somesthetic and proprioceptive information carried to both the sensory receiving cortex and the association cortex (Davidoff, 1990). 4. Conclusion Motor cortex stimulation was found to be effective in this particular patient with central pain following a TBI. As shown in our case, it is possible that doctors engaged in the the treatment and rehabilitation of a TBI might overlook the occurrence of central pain. Further detailed studies will be needed to determine the pathogenesis of central pain and the systematic analysis of the prevalence of central pain after a TBI. References Armand J. The origin, course and terminations of corticospinal fibers in various mammals. Prog Brain Res 1982;57:329–60. Berthier M, Starkstein S, Leiguarda R. Asymbolia for pain: a sensory– limbic disconnection syndrome. Ann Neurol 1988;24:41–9. Biemond A. The conduction of pain above the level of the thalamus opticus. Arch Neurol Psychiatry 1956;75:231–44. Boivie J. Hyperalgesia and allodynia in patients with CNS lesions. In: Willis WDJ, editor. Hyperalgesia and allodynia. New York: Raven Press; 1992. p. 363–73. Boivie J. Cental pain. In: Wall PD, Melzack R, editors. 4th ed. Textbook of pain. New York: Churchill Livingston; 1999. p. 879–914. Boivie J, Leijon G. Clinical findings in patients with central post-stroke pain. In: Casey KL, editor. Pain and central nervous system disease: the central pain syndromes. New York: Raven Press; 1991. p. 65–75. Bonica JJ. Semantic, epidemiologic, and educational issues of central pain. In: Casey KL, editor. Pain and central nervous system disease: the central pain syndromes. New York: Raven Press; 1991. p. 13–29. Craig AD, Bushnell MC, Zhang E-T, Blomqvist A. A thalamic nucleus specific for pain and temperature sensation. Nature 1994;372:770–3. Craig AD, Chen K, Bandy D, Reiman EM. Thermosensory activation of insular cortex. Nat Neurosci 2000;3:184–90. Craig AD, Reiman EM, Evans A, Bushnell MC. Functional imaging of an illusion of pain. Nature 1996;384:258–60. Craig AD, Zhang ET, Blomqvist A. A distinct thermoreceptive subregion of lamina I in nucleus caudalis of the owl monkey. J Comp Neurol 1999;404:221–34.
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Case report
Motor cortex stimulation for central pain following a traumatic brain injury Byung Chul Son b
a,*
, Sang Won Lee a, Eun Seok Choi b, Jae Hoon Sung a, Jae Taek Hong
a
a Department of Neurosurgery, St. Vincent’s Hospital, The Catholic University of Korea, Suwon, Republic of Korea Department of Rehabilitation, Daejeon St. Mary’s Hospital, The Catholic University of Korea, Daejeon, Republic of Korea
Received 5 August 2005; received in revised form 18 January 2006; accepted 21 February 2006
Abstract Central pain can occur in any lesions along the central nervous system affecting the spinothalamocortical pathway. Although diverse etiologies have been reported to cause central pain, there are few reports on the occurrence and surgical treatment of central pain following a traumatic brain injury (TBI). This paper describes the occurrence of central pain following a severe TBI, in which the diagnosis of central pain was typically delayed due to the patient’s decreased ability to express his pain for severe aphasia as a neurological sequela. The severe burning pain, deep pressure-like pain, and deep mechanical allodynia, which presented over the contralateral side to the TBI, were successfully relieved with motor cortex stimulation (MCS). The analgesic effect of stimulation was found to be long lasting and was still present at the 12-month follow up. As shown in this patient, the occurrence of central pain syndrome should be considered by physicians caring for TBI patients, and a comprehensive, systematic study will be needed to determine the prevalence of central pain after a TBI. Ó 2006 International Association for the Study of Pain. Published by Elsevier B.V. All rights reserved. Keywords: Central pain; Traumatic brain injury; Motor cortex stimulation
1. Introduction In 1994, central pain was defined by the International Association for the Study of Pain as ‘‘pain initiated or caused by a primary lesion or a dysfunction within the CNS’’ (Merskey and Bogduk, 1994). The reported causes of central pain are vascular lesions in the brain and spinal cord, multiple sclerosis, traumatic spinal cord injury, traumatic brain injury, syringomyelia and syringobulbia, tumors, abscesses, viral and syphilitic myelitis, epilepsy, and Parkinson’s disease. In addition to central pain caused by spontaneous lesions, surgical lesions of the central nervous system such as cordotomy also cause central pain. The highest prevalence of central pain has been observed to be a result of lesions in the spinal cord, *
Corresponding author. Tel.: +82 031 249 8202; fax: +82 031 245 5208. E-mail address: [email protected] (B.C. Son).
lower brainstem, and ventroposterior part of the thalamus (Bonica, 1991; Boivie, 1992; Tsubokawa and Katayama, 1998). Considering that traumatic brain injury (TBI) is a common cause of neurological morbidity around the world, and the spinal cord is a known lesion location, where the highest prevalence of central pain occurs, it is surprising that there are very few reports on the occurrence of central pain after a TBI (Boivie, 1999). There has been no clear explanation for this discrepancy of occurrence of central pain between brain and the spinal cord. Motor cortex stimulation (MCS) was first proposed for the treatment of central pain and has been shown to be effective in relieving peripheral neuropathic pain (e.g., trigeminal neuropathic pain, brachial plexus avulsion, and phantom pain) (Myerson et al., 1993; Tsubokawa et al., 1993; Nguyen et al., 1997; Tsubokawa and Katayama, 1998; Saitoh et al., 2000). According to
0304-3959/$32.00 Ó 2006 International Association for the Study of Pain. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.pain.2006.02.028
B.C. Son et al. / Pain 123 (2006) 210–216
a review of the literature, Nguyen et al. (1997) reported the result of MCS in one patient with central pain following a brain injury in 1997. However, the long-term results at 12 months were unsuccessful and the details were not reported. Because the report of central pain following a TBI is extremely rare, and medically intractable central pain conditions are notoriously resistant to treatment, we report a patient whose intractable central pain following TBI was successfully alleviated with MCS. 2. Case report 2.1. History and examination A 43-year-old right-handed man presented with a severe spontaneous burning pain in his right hand, forearm and right lower leg and foot, in addition to heaviness and deep pressure-like pain in his right lower leg including the foot. Two and a half years prior to admission, he fell from an electricity pole and sustained a severe TBI. Initially, he was comatose as a result of an acute subdural hematoma in his left convexity with multiple intracerebral contusions in his left temporal and frontoparietal lobe, he underwent an emergency decompressive craniectomy and an evacuation of the subdural hematoma and intracerebral hemorrhagic contusion. He was semicomatose after surgery and regained consciousness over a 1-month period after the injury. However, severe motor aphasia and a dense hemiplegia associated with a hemisensory deficit developed. During the subsequent 6 months, he was taken to the rehabilitation unit. His weakness progressively improved with active physical therapy, and finally he could stand and walk with assistance. Approximately 1 year after the accident, he could walk by himself slowly with a cane and a short leg prosthesis. However, he was hesitant to perform active exercise and finally refused to visit the rehabilitation unit. His wife who had been caring for him finally disclosed that he was suffering from a burning sensation and heaviness in his right lower leg and his arm. Indeed, he felt a gradually developing burning sensation in his right foot 6 months after the injury, which ascended slowly to the right upper leg, to the right inguinal area during the following 6 months, and deep pressure-like pain, heaviness, and crushing developed in his right leg. Approximately, one year after the accident he began to feel a burning pain in his right hand, which has ascended to his right forearm, and another area of burning developed in his right lower back. He also felt a deep pressure sensation in his right shoulder, which was regarded as a type of musculoskeletal pain associated with a frozen shoulder. Because of the progressive difficulty in performing exercise and his withdrawal response, he underwent a careful interview and sensory
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examination. As a result, he was finally diagnosed with a central pain following a TBI approximately 18 months after the accident and 1 year after the development of pain. After the central pain had been diagnosed, the maximum medical treatment was provided for 3 months but, his pain progressively worsened. The burning sensation in his leg and arm was constant, and he experienced an intermittent cramping pain. His pain was aggravated as a result of exposure to cold temperatures, humidity, and emotional upsets. During the 2 months prior to referral, he could barely sleep at night, stroking his right leg and right hand due to the severe heaviness and burning. His pain medication regimen at the time of referral was as follows: gabapentin 2400 mg, paroxetine 20 mg, tramadol 200 mg, trazodon 25 mg, oxycarbamazepine 600 mg, and amitryptyline 30 mg a day. At the time of referral, his VAS was 75–85/100. A physical examination showed that he had residual motor weakness (grade 4/4) which was more severe in the distal arm and leg. He showed a hemiplegic gait and moderate rigidity in his arm and leg, he could walk by himself slowly and carefully in a guarded fashion. Hypesthesia to light touches in addition to pinprick hypoalgesia, which was more severe in the painful areas, was present on his right hemibody including face. In his right arm and leg, i.e., the painful areas, there was decreased thermal sensation, particularly cold. There was a severe mechanical deep pressure allodynia in his right leg and foot. However, no spontaneous paresthesia and other types of mechanical allodynia, such as static, dynamic, and cold allodynia were found. Fig. 1 shows the distribution of his pain and sensory deficits. His mentality was clear without confusion and disorientation. However, severe motor aphasia with stuttering was noticed and his speech was difficult to understand. He had difficulty in naming and showed some shortterm memory impairment. The magnetic resonance imaging showed extensive damage to the left frontal, temporal, insular, and parietal lobe (Fig. 2). Severe encephalomalacic changes to the posterior part of inferior frontal gyrus, were thought to be the cause of motor aphasia. 2.2. Surgical procedure An anatomical localization of the central sulcus was performed using a three-dimensional image-guided navigation system. After marking the course of the central sulcus over the left convexity and the vertex, an approximately 10-cm-long linear incision was carried out, and an approximately 7-cm-diameter craniotomy was performed under general anesthesia. The surgical procedure performed in this patient was similar to those reported previously (Nguyen et al., 1997; Katayama et al., 1998; Tsubokawa and Katayama, 1998; Son et al., 2003).
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as a ‘hand knob’ (Yousry et al., 1997), and this electrode was placed subdurally along the mediolateral somatotopy of the precentral gyrus because the overlying dura mater was thickened as a result of previous trauma surgery. Another electrode for stimulating the lower leg was placed epidurally, parallel to the course of the superior sagittal sinus, as recommended elsewhere (Fig. 3) (Katayama et al., 1998; Tsubokawa and Katayama, 1998). During the 7-day test stimulation period, significant pain relief was observed when a 21 Hz, 210 ms, 0.8–1.2 V (‘‘0’’ negative, ‘‘3’’ positive, continuous mode) for the forearm electrode and 30 Hz, 210 ms, 2.0–2.5 V (‘‘0’’ negative, ‘‘2’’ positive, continuous mode) for the leg and foot stimulation combinations were used. During stimulation, a warm, vibrating paresthesia was produced in his right hand, forearm, right lower trunk, and his lower leg including the foot. Two pulse generators (Itrel IIIÒ, model 7425, Medtronic Inc., Minneapolis, MN) were implanted in each side of the upper chest after the induction of anesthesia (Fig. 3). 2.3. Results of pain relief
Fig. 1. Schematic diagram showing the distribution of central pain after a TBI. The horizontally hatched areas indicate severe spontaneous burning pain. The obliquely hatched area shows heaviness and pressure-like squeezing pain. Hypesthesia and hypoalgesia to a pinprick were noted in the right side of the body including face.
We were unable to obtain an adequate motor contraction with direct cortical stimulation up to 18 mA used to identify the neurophysiological somatotopy of the precentral gyrus despite the discontinuation of the muscle relaxant well before beginning the direct precentral gyrus stimulation with a bipolar cortical stimulator. Therefore, the location of the stimulating electrode (Resume IIÒ, model 3587A, Medtronic Inc., Minneapolis, MN) for the hand and forearm was determined according to the anatomical imaging landmark indicating a motor hand area that was previously described
The level of stimulation was adjusted until satisfactory pain relief had been achieved by setting the electrodes at 21–30 Hz, 210 ms, and 0.8–2.4 V. The post-stimulation analgesic effect was estimated to last approximately 5 min, and a continuous mode of stimulation was delivered. Visual analogue scales, which were graduated from 0 to 100, were used to assess the extent of pain relief. However, the McGill Pain Questionnaire could not be assessed in this patient due to severe aphasia (Melzack, 1975). The effect of stimulation was evaluated preoperatively and 12 months post-operatively. The visual analogue scale score improved 75–85 to 20–30 with stimulation, and the spontaneous burning pain in the right forearm, hand, and lower trunk improved by 90–95%. The burning pain, heaviness, and deep pressure-like pain in his right leg improved by 70–80%. However, the heaviness and deep pressure allodynia in his foot improved by only 50%. The patient’s pain changed minimally over the 12 months of follow up. The shoulder pain previously believed to be a type of musculoskeletal pain also improved and the range of motion in his right shoulder increased much more with the alleviation of pain, he could elevate his shoulder again. An unwanted motor contraction and seizure activity was not been observed. After 12 months of stimulation, the patient’s medication was decreased to 900 mg gabapentin and 10 mg amitriptyline per day. 3. Discussion Although head trauma had been reported to be a cause of central pain, there are few reports on the
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Fig. 2. Radiological findings showing the anatomical location of central pain following a TBI. (A) T1-weighted magnetic resonance image shows that extensive damage to the insular cortex and perisylvian temporoparietal opercular areas. Note the severe loss of the insular cortex and the underlying white matter, which interferes with the thalamocortical transfer of nociceptive information. (B) T1-weighted magnetic resonance image demonstrates additional damage to the post-central gyrus and white matter in the parietal lobe.
occurrence of central pain after a TBI (Berthier et al., 1988; Boivie, 1999; Yezierski, 2002). Until now, it is uncertain why TBI causes central pain so rarely.
Fig. 3. Post-operative skull X-ray image showing the placement of the two laminotomy electrodes in the left hemisphere. There are two previous craniotomy sites on each side of the calvarium and a new craniotomy for the placement of an electrode for motor cortex stimulation.
However, it is possible that central pain itself is often overlooked as a possibility in patients with a CNS disease because of a lack of knowledge of its characteristics (Boivie, 1999). This may cause puzzling symptoms when several coexisting pains of an unusual nature exist. One reason for the lack of knowledge of central pain is the fact that relatively little systematic research has been carried out on the clinical aspects of central pain. In addition, the lack of experimental models for central pain until recently hampered research into its mechanisms (Boivie, 1999). Burning pain and deep pressure-like pain in this patient localized within the region of hypoesthesia and he showed severe deficits in his ability to detect pain and cold, as well as clear deficits in touch and proprioception. Thus, this patient with central pain due to TBI showed a clinical picture similar to CPSP. CPSP patients generally have clear somatosensory deficits and a paradoxical ongoing spontaneous pain that is felt within the area of deficit. Central pain can be experienced as superficial or deep pain, or both superficial and deep components, but the high incidence of cutaneous hyperesthesias contributes to the impression that superficial pain dominates, although deep pain is common too. In this particular patient, only mechanical deep pressure allodynia was noted. In CPSP, cutaneous hyperalgesia, allodynia, and/or hyperpathia are frequently, but not invariably, present (Boivie and Leijon, 1991; Boivie, 1999). Recently, dissociation between cutaneous and deep sensibility in CPSP has been reported (Mailis and Bennett, 2002). Several areas of the brain, fronto-temporal and insular, and parietal lobes in this patient were severely damaged (Fig. 2). Among them, the areas particularly
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related to the pathophysiology of central pain are the insular and parietal lobes. The parietal or insular regions have been shown to be associated with central pain (Michel et al., 1990; Schmahmann and Leifer, 1992; Boivie, 1999). Schmahmann and Leifer (1992) studied the anatomic correlations in 6 patients with central pain as a result of lesions of the parietal lobe, and reported that the common area of involvement in their cases was the white matter deep to both the caudal insula and the opercular region of the posterior parietal cortex. They suggested that a disruption of the interconnections between these cerebral cortical areas (including the second somatosensory representation, SII) and the thalamus, particularly the intralaminar and ventroposterior nuclei, might be responsible for the occurrence of central pain syndrome namely, parietal pseudothalamic pain syndrome. The extensive area of damage to the insula in this patient was consistent with those reported by Schmahmann and Leifer (1992). The middle/posterior insular cortex is known to be the area where discriminative thermosensory sensation is represented in humans (Craig et al., 2000). The functional anatomy in monkeys indicates that a dedicated thalamic nucleus relays the topographic, discriminative thermoreceptive-specific, and nociceptive-specific lamina I spino- and trigeminospecific projections to the dorsal margin of the middle/posterior insular cortex (Craig et al., 1994, 1999). Data from a PET imaging study of a thermal grill illusion of pain and an fMRI study indicate that a strong innocuous cool stimulation (20 °C) activates the contralateral insular cortex, but not the parietal cortex (Craig et al., 1996; Davis et al., 1999). These findings support the proposal that central pain results from loss of the normal inhibition of pain by cold (Craig et al., 1994, 2000), because the lesions involving the insula can produce central pain (Schmahmann and Leifer, 1992). The parietal opercular area including the SII was also damaged in our patient (Fig. 2B). Lesions of the SII and the insula produce asymbolia for pain, suggesting that the SII is an important cortical locus for the conscious perception of noxious stimuli (Biemond, 1956; Mesulam and Mufson, 1985; Berthier et al., 1988). The anatomical and electrophysiological data show that in monkeys, these regions receive direct nociceptive input (Ploner et al., 1999; Craig et al., 2000). Experimental and lesion data in humans suggest these areas are associated with the motivational-affective aspects of pain and the sensory-discriminative components of pain perception (Vogt et al., 1993; Craig et al., 1996; Rainville et al., 1997; Ploner et al., 1999). Although MCS has been proven to be a promising treatment for various central and peripheral neuropathic pain, the precise analgesic mechanism of MCS is still unclear (Garcı´a-Larrea et al., 1997; Nguyen et al., 1997; Katayama et al., 1998). Tsubokawa and Katayama
have suggested that MCS might produce an analgesic effect through the orthodromic and/or antidromic activation of the fourth-order antinociceptive neurons, which secondarily results in the inhibition of hyperactive nociceptive cortical neurons, that restores the inhibitory surrounding field around the restricted area of excited neurons in the somatosensory cortex (Tsubokawa et al., 1993). However, MCS has not been shown to produce any significant cerebral blood flow (CBF) changes in the parietal cortex, suggesting that the sensory cortex is not the key structure (Peyron et al., 1995; Garcı´a-Larrea et al., 1999; Nguyen et al., 1999). On the other hand, positron emission tomography (PET) studies suggest that the thalamus is an important structure in the mediation of the functional MCS effects, and MCS exerts its analgesic effect by modulating the thalamic activity (Nguyen et al., 1999; Son et al., 2003; Saitoh et al., 2004). Studies on groups of patients with intractable pain with various origins have confirmed the existence of significant CBF increases during MCS in the lateral and medial thalamus, anterior cingulate-orbitofrontal cortex (BA32), the anterior insula-medial temporal lobe, and the upper brainstem (Garcı´a-Larrea et al., 1997). The thalamic area showing the most significant CBF changes are the ventrolateral and ventroanterior nuclei, i.e., the thalamic regions directly connected to the motor and premotor cortices. However, these clinical and PET studies could not explain how MCS relieves the CPSP, which has a damaged thalamus, where the substrate for the functioning MCS has already been destroyed by the stroke. Recently, Saitoh et al. (2004) showed in a patient with CPSP that was caused by a thalamic hemorrhage that a successful MCS induced a significant CBF increase in the contralateral hemisphere (thalamus, gyrus rectus, and superior frontal cortex) compared with the stimulated one, suggesting that the efficacy of MCS was mainly related to the increased synaptic activity in the thalamus. As an explanation for the contralateral thalamic activation, they suggested that the reorganization of the major thalamic function to the contralateral side and the contralateral thalamus in the dominant hemisphere might play a more important role in their particular patient. It has already been reported that right post-stroke pain disappeared after an additional contralateral left parietal lobe lesion (Helmchen et al., 2002). It is now known that only approximately 1/2 of the pyramidal tract fibers, which are those constituting the corticospinal tract itself, actually terminate in the spinal cord (Wisendanger, 1969; Davidoff, 1990). Many pyramidal tract axons terminate in, or send collateral branches to, a number of supraspinal structures that are generally considered to be sensory in function (e.g., sensory and motor nuclei of the thalamus, trigeminal
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