Mechanism of trigeminal neuralgia: an ultrastructural analysis of trigeminal root specimens obtained during microvascular decompression surgery

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Object. Recent progress in the understanding of abnormal electrical behavior in injured sensory neurons motivated an examination, at the ultrastructural level, of trigeminal roots of patients with trigeminal neuralgia (TN).

Methods. In 12 patients biopsy specimens of trigeminal root were obtained during surgery for microvascular decompression. Pathological changes in tissue included axonopathy and axonal loss, demyelination, a range of less severe myelin abnormalities (dysmyelination), residual myelin debris, and the presence of excess collagen, including condensed collagen masses in two cases. Within zones of demyelination, groups of axons were often closely apposed without an intervening glial process. Pathological characteristics of nerve fibers were clearly graded with the degrees of root compression noted at operation. Pain also occurred, however, in some patients who did not appear to have a severe compressive injury.

Conclusions. Findings were consistent with the ignition hypothesis of TN. This model can be used to explain the major positive and negative symptoms of TN by axonopathy-induced changes in the electrical excitability of afferent axons in the trigeminal root and of neuronal somata in the trigeminal ganglion. The key pathophysiological changes include ectopic impulse discharge, spontaneous and triggered afterdischarge, and crossexcitation among neighboring afferents.

Article Information

Address reprint requests to: Marshall Devor, Ph.D., Institute of Life Sciences, Hebrew University, Jerusalem 91904, Israel. email: marshlu@vms.huji.ac.il.

© AANS, except where prohibited by US copyright law.

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Figures

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    Case 4. Documentation of pathological changes in the trigeminal root of a patient who underwent MVD surgery for relief of typical TN. Upper: Schematic representation of the relation of the biopsy sample to the trigeminal sensory root and compressing arterial loop (left) and light photomicrograph of the biopsy sample (right). Lower: Electron micrographs showing a zone of dysmyelination (left, note the plentiful collagen [white areas]) and a zone of demyelination (right) with abundant myelin debris. Arrows (thick and thin) indicate approximate locations represented in the electron micrographs. The thick arrow indicates the external (inferior) root surface that was adjacent to the compressing arterial loop. The thin arrow indicates the torn surface of the specimen, an area that was located in the interior of the root in situ. Bars: upper, 200 µm; lower, 5 µm.

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    Electron micrographs demonstrating tissue disorganization in trigeminal root biopsy samples. A: Case 4. Central zone of demyelination with residual myelin debris surrounded by dysmyelination. Note the swollen axons with thin compact myelin on the left. B: Case 5. Large myelin sheath containing numerous axon profiles of regenerating sprouts. C: Case 6. Cluster of demyelinated axons in close membrane-to-membrane contact (including where indicated by arrows). Many additional clusters of this sort are visible in A. Bars: A, 5 µm; B and C, 2 µm.

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    A–C: Case 6. Photomicrographs of serial semithin sections from a trigeminal root biopsy sample in which a collagen mass was present (arrow) and surrounded by a zone of demyelination. D: Schematic reconstruction of the sample as it would appear in situ. Letters A–C indicate the approximate locations of the areas shown in the three corresponding photomicrographs. E–G: Electron micrographs (E and F) and photomicrograph (G) documenting that the mass consisted of nearly pure collagen. A longitudinal view of a collagen fibril within the mass, showing characteristic collagen striations (E); collagen fibrils in cross section (F); and a semithin tissue section stained for collagen (G). Bars: A–C and G, 200 µm; E and F, 0.5 µm.

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    Electron micrographs demonstrating relatively intact tissue to provide a comparison for regions of trigeminal root compression. A: Case 6. Spared edge of a trigeminal root biopsy sample. There was heavy de- and dysmyelination located more centrally in this sample (Figs. 2C and 3C). Most axons are relatively intact, but in some there is expansion of the inner (asterisk) or outer (upper left) mesaxon, or myelin invagination (upper right). B: Trigeminal root biopsy sample from a healthy rat. This sample was dissected and fixed by immersion just like the human trigeminal biopsy samples. Most axons are intact, but at least one (asterisk) shows cytoplasmic expansion within the compact myelin (presumably at an incisure), and several show minor delamination and myelin invaginations. C: Sample of a C-2 dorsal root from a patient who underwent C-2 ganglionectomy for the treatment of intractable headache. Bar: 5 µm (for all images).

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