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Segmental, Axonal, and Demyelinative Lesions in the Trigeminal System Produce Neuropathic Pain

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Segmental, Axonal, and Demyelinative Lesions in the Trigeminal System Produce Neuropathic Pain Segmental, Axonal, and Demyelinative Lesions in the Trigeminal System Produce Neuropathic Pain William R. Bauer, M.D. Medical College of Ohio 2005 DEDICATION To my wife Kate, my family, and patients, may they all suffer less pain. ii TABLE OF CONTENTS INTRODUCTION…………………………………………………………………...……1 LITERATURE REVIEW………………………………………………………...............5 CHAPTER 1: Loose Infraorbital Nerve Ligatures Do Not Produce Neuropathic Pain……………………………………………………………….….19 CHAPTER 2: Behavioral and Immunocytochemical Evidence of Trigeminal Neuropathic Pain Produced by a Partial Infraorbital Nerve Lesion........……....…43 CHAPTER 3: Behavioral Evidence of Glycerol Induced Trigeminal Neuropathic Pain in Sprague-Dawley Rats……………………………………………………..74 DISCUSSION/SUMMARY……………………………………………………………110 REFERENCES…………………………………………………………………………119 ABSTRACT…………………………………………………………………………….154 iii INTRODUCTION One would expect that damage to a sensory nerve would produce sensory loss with the degree of loss roughly proportional to the amount of damage. This is the usual result. Sometimes, when peripheral somatosensory nerves are damaged by disease or trauma, a small percentage of cases develop positive symptoms. These symptoms are almost always various kinds of pain rather than numbness or tingling. The pain is said to be neuropathic because it is believed to be due to a dysfunctional nervous system. Neuropathic pain (NP) is commonly observed in the location of the primary sensory neuron as opposed to a more peripheral location. Neuropathic pain is considered to be a serious clinical problem that remains poorly understood and poorly treated by many physicians. The International Association for the Study of Pain (IASP) defines NP as “pain initiated or caused by a primary lesion or dysfunction in the nervous system” (Merskey and Bogduk, 1994). The IASP defines pain as “an unpleasant sensory and emotional experience associated with actual or potential tissue damage, or described in terms of such damage.” The etiologic classification of NP covers a variety of disease states including phantom limb, spinal cord injury, late-stage cancer, painful diabetic neuropathy, post-herpetic neuralgia, HIV, vinca-alkaloids, sciatica, multiple sclerosis, atypical facial pains, and trigeminal neuralgia (TN). Neuropathic pain frequently becomes chronic in nature. Chronic pain (CP) is among the most disabling and costly afflictions in North America, Europe, and Australia. The IASP 1 provides a widely used definition of CP as “pain without apparent biologic value that persisted beyond the normal tissue healing time” (usually taken to be 3 mos.). The prevalence rate of CP was recently reviewed by the IASP (2003) in 13 studies and ranged from 10.1% to 55.2%. There is clinically significant CP found in 65% of persons diagnosed with multiple sclerosis (MS). These painful conditions include TN, painful optic neuritis and Lehrmitte’s syndrome (Kerns et al., 2002). Trigeminal neuralgia is a well-recognized complication of MS and is thought to be due to plaques of demyelination in the trigeminal root entry zone, or less commonly, the brainstem (Jensen et al., 1982; Moulin et al., 1988; Soustiel et al., 1996; Moulin, 1998). The examination by several laboratory groups of trigeminal rhizotomy specimens from patients with MS and intractable TN in the absence of a trigeminal compressive lesion reveal that demyelination has been found to extend along the proximal part of the trigeminal nerve root, in some cases right up to the junction with the peripheral nervous system (Love et al., 2001; Lazar and Kirkpatrick, 1979; Hilton et al., 1994). Moreover, many of these rhizotomy specimens reportedly exhibited inflammatory disease activity, as evidenced by the presence of lipid-laden macrophages. Another finding in most of these specimens is the closely juxtaposed bundles of thinly myelinated axons (Love et al., 2001). As there is good experimental evidence that ectopic impulses can arise from demyelinated axons (Rasminsky, 1978; Smith and McDonald, 1980, 1982), it is possible that the pathophysiology of TN is due to hyperactivity or abnormal discharges arising from the trigeminal ganglion (Moller, 1991; Burchiel, 1993; Pagni, 1993; Rappaport and Devor, 1994; Moulin, 1998). It is also possible that the abnormal generation of sensory 2 impulses from fibers conveying light touch to fiber pathways involved in the perception of pain, could cause the pathophysiologic effects of TN. It is more likely a combination of these effects contribute to the symptomatology of any given patient with TN. While it is important to diagnose the spectrum of disease conditions that can result in NP, disease diagnosis by itself is seldom helpful in selecting the optimal pain therapy. An important facet of the pain diagnosis is the proper identification of the neurobiological mechanisms responsible for neuropathic pain. The use of a mechanism-based approach to this condition offers the possibility of greater diagnostic sensitivity and a more rational basis for therapy. Trigeminal neuralgia probably involves peripheral sensitization, alteration of ion channel expression, ectopic and spontaneous discharge, ephaptic conduction and sprouting of sympathetic axons into the gasserian ganglion. Central sensitization, cortical reorganization, spinal reorganization, and changes in inhibitory pathways are also likely to be involved in NP syndromes. These mechanisms reveal the complex nature of the response to any peripheral nerve injury. Current knowledge of peripheral, spinal, and brain events following disease or trauma suggest that many mechanistic aspects are involved in NP syndromes. The study of the mechanisms central to NP, especially that seen in patients with TN, is fundamental to the development of new therapies. The overall goals of this dissertation project were to characterize three specific models of pain in the trigeminal system of the rat and evaluate the lesion site pathology associated with each model for evidence of changes that may contribute to the nature and 3 persistence of NP. Experimental methods used in these studies included anatomical pathology and behavioral measures in the male adult rat. The pain models used in these studies were chronic loose circumferential ligatures of the trigeminal infraorbital nerve (ION), tight partial trigeminal ION ligature, and glycerol injection into the trigeminal ganglion. 4 LITERATURE REVIEW One of the most common and debilitating clinical sensory disorders that can result from injury to primary afferent neurons is pain from mechanical contact with the skin (Bonica, 1990). Normally non-noxious stimuli such as brushing against clothing, or a puff of air might now elicit pain (tactile allodynia), however stimuli with sharp features, such as a stiff bristle, or the rough surface of sandpaper, will elicit considerable pain that outlasts the stimulus (mechanical hyperalgesia). In addition to chronic, spontaneous NP, the mechanical dysesthesia of allodynia and hyperesthesia are most troublesome because of our daily need to interact with objects in our environment. Given that these are the most common types of pain seen in clinical practice, elucidation of their mediators in the somatic or the trigeminal distribution of sensory nerve fibers, and their cellular sources and mechanisms of action is not only of scientific interest but also of significant clinical relevance. Knowledge of the neuroanatomy of the somatosensory system is necessary for a clear understanding of the pathophysiology and mechanisms of NP. The anatomical pathways which transmit vision or hearing to the central nervous system normally involve four main components. These components include transduction of physical into electrical energy (receptor), the integration of the electrical signal (somal trigger zone), the conducting axon, and the signal output (synapse). Sensory signals are received by the receptor, which is a specialized structure that aids in the recognition and initiation of signal transmission. The receptor or generator potential is the transforming event that 5 changes the various stimuli (e.g. pressure, touch, temperature) into electrical and chemical signals for transmission. Signal integration occurs at the trigger zone whereby an action potential can be generated and sent down the axon. The action potential is transmitted centrally via the axon to the pre-synaptic terminal where it signals chemical transmitters to be released from vesicles into the synapse and then diffuse to the post- synaptic site on the central post-synaptic terminal. Binding of the neurotransmitter at the post-synaptic receptor permits additional signals to be generated and sent to thalamus and sensory cortex. The ION of the trigeminal ganglion, like other sensory nerves, is composed of axons of different diameters and degrees of myelination. These axons convey modality specific signals, such as nociception, thermoreception, mechanoreception, and proprioception at different velocities to distinct second-order terminations in the brainstem nuclei. The main types of primary sensory afferents include the Aα-, Aβ-, Aδ-, and C-type fibers. Table I provides a summary of fiber diameter, conduction velocity, presence of myelin and stimuli for activating these fibers (Martin, 1985; Fields, 1987). Note that diameter and conduction velocity will vary from species to species. These examples are from initial work done in the cat (Gasser, 1960; Burgess and Perl, 1973). The variation in axon diameter and myelination affects the conduction properties
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