International Journal of Oral Biology

The Korean Academy of Oral Biology (대한구강생물학회)
권호 표지

Trigeminal Neuralgia like Pain Behavior Following Compression of the Rat Trigeminal Ganglion

  • Yang, Gwi-Y. (Department of Oral Physiology, School of Dentistry, Kyungpook National University) ;
  • Mun, Jun-H. (Department of Oral Physiology, School of Dentistry, Kyungpook National University) ;
  • Park, Yoon-Y. (Department of Physiology, School of Medicine, Catholic University of Daegu) ;
  • Ahn, Dong-K. (Department of Oral Physiology, School of Dentistry, Kyungpook National University)
  • Published : 2009.09.30
Download PDF
⟨ Previous Next ⟩

Abstract

We recently described a novel animal model of trigeminal neuropathic pain following compression of the trigeminal ganglion (Ahn et al., 2009). In our present study, we adapted this model using male Sprague-Dawley rats weighing between 250-260 g and then analyzed the behavioral responses of these animals following modified chronic compression of the trigeminal ganglion. Under anesthesia, the rats were mounted onto a stereotaxic frame and a 4% agar solution ($10{\mu}L$) was injected in each case on the dorsal surface of the trigeminal ganglion to achieve compression without causing injury. In the control group, the rats received a sham operation without agar injection. Air-puff, acetone, and heat tests were performed at 3 days before and at 3, 7, 10, 14, 17, 21, 24, 30, 40, 55, and 70 days after surgery. Compression of the trigeminal ganglion produced nociceptive behavior in the trigeminal territory. Mechanical allodynia was established within 3 days and recovered to preoperative levels at approximately 60 days following compression. Mechanical hyperalgesia was also observed at 7 days after compression and persisted until the postoperative day 40. Cold hypersensitivity was established within 3 days after compression and lasted beyond postoperative day 55. In contrast, compression of the trigeminal ganglion did not produce any significant thermal hypersensitivity when compared with the sham operated group. These findings suggest that compression of the trigeminal ganglion without any injury produces prolonged nociceptive behavior and that our rat model is a useful system for further analysis of trigeminal neuralgia.

Keywords

References

  1. Adams CBT. Microvascular compression: an alternative view and hypothesis. J Neurosurg. 57:1-12, 1989 https://doi.org/10.3171/jns.1989.70.1.0001
  2. Ahn DK, Lee SY, Han SR, Ju JS, Yang GY, Lee MK, Youn DH, Bae YC. Intratrigeminal ganglionic injection of LPA causes neuropathic pain-like behavior and demyelination in rats. Pain. 2009, in press. doi:10.1016/j.pain.2009.07.012
  3. Ahn DK, Jung CY, Lee HJ, Choi HS, Ju JS, Bae YC. Peripheral glutamate receptors participate in interleukin-1beta-induced mechanical allodynia in the orofacial area of rats. Neurosci Lett. 357:203-6, 2004 https://doi.org/10.1016/j.neulet.2003.12.097
  4. Ahn DK, Kim KH, Jung CY, Choi HS, Lim EJ, Youn DH, Bae YC. Role of peripheral group I and II metabotropic glutamate receptors in IL-1$\beta$-induced mechanical allodynia in the orofacial area of conscious rats. Pain. 118:53-60, 2005b https://doi.org/10.1016/j.pain.2005.07.017
  5. Ahn DK, Lim EJ, Kim BC, Yang GY, Lee MK, Ju JS, Han SR, Bae YC. Compression of the trigeminal ganglion produces prolonged nociceptive behavior in rats. Eur J Pain. 13:568-75, 2009 https://doi.org/10.1016/j.ejpain.2008.07.008
  6. Benoliel R, Wilensky A, Tal M, Eliav E. Application of a proinflammatory agent to the orbital portion of the rat infraorbital nerve induces changes indicative of ongoing trigeminal pain. Pain 99:567-78, 2002 https://doi.org/10.1016/S0304-3959(02)00272-5
  7. Briggs CA, Chandraraj S. Variations in the lumbosacral ligament and associated changes in the lumbosacral region resulting in compression of the fifth dorsal root ganglion and spinal nerve. Clin Anat. 8:339-46, 1995 https://doi.org/10.1002/ca.980080506
  8. Choi Y, Yoon YW, Na HS, Kim SH, Chung JM. Behavioral signs of ongoing pain and cold allodynia in a rat model of neuropathic pain. Pain. 59:369-76, 1994 https://doi.org/10.1016/0304-3959(94)90023-X
  9. Claiborne J, Nag S, Mokha SS. Activation of opioid receptor like-1 receptor in the spinal cord produces sex-specific antinociception in the rat: estrogen attenuates antinociception in the female, whereas testosterone is required for the expression of antinociception in the male. J Neurosci. 26:13048-53, 2006 https://doi.org/10.1523/JNEUROSCI.4783-06.2006
  10. Dandy DW. Concerning the cause of trigeminal neuralgia. Am J Surg. 24:447-55, 1934 https://doi.org/10.1016/S0002-9610(34)90403-7
  11. Devor M, Amir R, Rappaport ZH. Pathophysiology of trigeminal neuralgia: the ignition hypothesis. Clin J Pain. 18:4-13, 2002a https://doi.org/10.1097/00002508-200201000-00002
  12. Devor M, Govrin-Lippmann R, Rappaport ZH. Mechanism of trigeminal neuralgia: an ultrastructural analysis of trigeminal root specimens obtained during microvascular decompression surgery. J Neurosurg. 96:532-43, 2002b https://doi.org/10.3171/jns.2002.96.3.0532
  13. Gardner WJ. Concerning the mechanism of trigeminal neuralgia and hemifacial spasm. J Neurosurg. 19:947-58, 1965 https://doi.org/10.3171/jns.1962.19.11.0947
  14. Fields HL. Treatment of trigeminal neuralgia. N Engl J Med. 334:1125-6, 1996 https://doi.org/10.1056/NEJM199604253341709
  15. Hilton DA, Love S, Gradidge T, Coakham HB. Pathological findings associated with trigeminal neuralgia caused by vascular compression. Neurosurgery. 35:299-303, 1994 https://doi.org/10.1227/00006123-199408000-00017
  16. Hu SJ, Xing JL. An experimental model for chronic compression of dorsal root ganglion produced by intervertebral foramen stenosis in the rat. Pain. 77:15-23, 1998 https://doi.org/10.1016/S0304-3959(98)00067-0
  17. Imamura Y, Kawamoto H, Nakanishi O. Characterization of heat-hyperalgesia in an experimental trigeminal neuropathy in rats. Exp Brain Res. 116:97-103, 1997 https://doi.org/10.1007/PL00005748
  18. Jannetta PJ. Arterial compression of the trigeminal nerve at the pons in patients with trigeminal neuralgia. J Neurosurg. 26:159-62, 1967 https://doi.org/10.3171/jns.1967.26.1part2.0159
  19. Jung CY, Choi HS, Ju JS, Park HS, Kwon TG, Bae YC, Ahn DK. Central metabotropic glutamate receptors differentially participate in IL-1β-induced mechanical allodynia in the orofacial area of conscious rats. J Pain. 7:747-56, 2006 https://doi.org/10.1016/j.jpain.2006.03.007
  20. Lim EJ, Jeon HJ, Yang GY, Lee MK, Ju JS, Han SR, Ahn DK. Intracisternal administration of mitogen-activated protein kinase inhibitors reduced mechanical allodynia following chronic constriction injury of infraorbital nerve in rats. Prog Neuropsychopharmacol Biol Psychiatry. 31:1322-9, 2007 https://doi.org/10.1016/j.pnpbp.2007.05.016
  21. Love S, Coakham HB. Trigeminal neuralgia: pathology and pathogenesis. Brain. 124:2347-60, 2001 https://doi.org/10.1093/brain/124.12.2347
  22. Lovely TJ, Jannetta PJ. Microvascular decompression for trigeminal neuralgia. Surgical technique and long-term results. Neurosurg Clin N Am. 8:11-29, 1997
  23. Kitt CA, Gruber K, Davis M, Woolf CJ, Levine JD. Trigeminal neuralgia: opportunities for research and treatment. Pain. 85:3-7, 2000 https://doi.org/10.1016/S0304-3959(99)00310-3
  24. McLaughlin MR, Jannetta PJ, Clyde BL, Subach BR, Comey CH, Resnick DK. Microvascular decompression of cranial nerves: lessons learned after 4400 operations. J Neurosurg. 90:1-8, 1999 https://doi.org/10.3171/jns.1999.90.1.0001
  25. Park CK, Kim K, Jung SJ, Kim MJ, Ahn DK, Hong SD, Kim JS, Oh SB. Molecular mechanism for local anesthetic action of eugenol in the rat trigeminal system. Pain. 144:84-94, 2009 https://doi.org/10.1016/j.pain.2009.03.016
  26. Poletti CE. Third cervical nerve root and ganglion compression: clinical syndrome, surgical anatomy, and pathological findings. Neurosurgery. 39:941-8, 1996 https://doi.org/10.1097/00006123-199611000-00012
  27. Sindrup SH, Jensen TS. Pharmacotherapy of trigeminal neuralgia. Clin J Pain. 18:22-7, 2002 https://doi.org/10.1097/00002508-200201000-00004
  28. Song XJ, Hu SJ, Greenquist KW, Zhang JM, LaMotte RH. Mechanical and thermal hyperalgesia and ectopic neuronal discharge after chronic compression of dorsal root ganglia. J Neurophysiol. 82:3347-58, 1999
  29. Tall JM, Stuesse SL, Cruce WL, Crisp T. Gender and the behavioral manifestations of neuropathic pain. Pharmacol Biochem Behav. 68:99-104, 2001 https://doi.org/10.1016/S0091-3057(00)00461-5
  30. Vos BP, Hans G, Adriaensen H. Behavioral assessment of facial pain in rats: face grooming patterns after painful and non-painful sensory disturbances in the territory of the rat's infraorbital nerve. Pain. 76:173-8, 1998 https://doi.org/10.1016/S0304-3959(98)00039-6
  31. Vos BP, Strassman AM, Maciewicz RJ. Behavioral evidence of trigeminal neuropathic pain following chronic constriction injury to the rat's infraorbital nerve. J Neurosci. 14:2708-23, 1994
  32. Yang CS, Jung CY, Ju JS, Lee MK, Ahn DK. Intracisternal administration of mitogen-activated protein kinase inhibitors reduced IL-1beta-induced mirror-image mechanical allodynia in the orofacial area of rats. Neurosci Lett. 387:32-7, 2005 https://doi.org/10.1016/j.neulet.2005.07.019
  33. Yang GY, Park YH, Lee MK, Kim SK, Ahn DK. Compression of the trigeminal ganglion enhances nociceptive behavior produced by formalin in the orofacial area of rats. International Journal of Oral Biology. 33:155-62, 2008
  34. Zakrzewska JM, Lopez BC, Kim SE, Coakham HB. Patient reports of satisfaction after microvascular decompression and partial sensory rhizotomy for trigeminal neuralgia. Neurosurgery. 56:1304-11, 2005 https://doi.org/10.1227/01.NEU.0000159883.35957.E0
  35. Zakrzewska JM, Patsalos PN. Drugs used in the management of trigeminal neuralgia. Oral Surg Oral Med Oral Pathol. 74:439-50, 1992 https://doi.org/10.1016/0030-4220(92)90292-X