Journal of Korean Neurosurgical Society

The Korean Neurosurgical Society (대한신경외과학회)
권호 표지
DOI QR코드

DOI QR Code

Cold Allodynia after C2 Root Resection in Sprague-Dawley Rats

  • Chung, Daeyeong (Department of Neurosurgery, Cham Teun Teun Hospital) ;
  • Cho, Dae-Chul (Department of Neurosurgery, Kyungpook National University Hospital) ;
  • Park, Seong-Hyun (Department of Neurosurgery, Kyungpook National University Hospital) ;
  • Kim, Kyoung-Tae (Department of Neurosurgery, Kyungpook National University Hospital) ;
  • Sung, Joo-Kyung (Department of Neurosurgery, Kyungpook National University Hospital) ;
  • Jeon, Younghoon (Department of Anesthesiology and Pain Medicine, School of Dentistry, Kyungpook National University)
  • Received : 2017.04.27
  • Accepted : 2017.09.06
  • Published : 2018.03.01
Download PDF
⟨ Previous Next ⟩

Abstract

Objective : The purpose of this study was to evaluate pain-related behaviors after bilateral C2 root resection and change in pain patterns in the suboccipital region in rats. Methods : Male Sprague-Dawley rats were randomly assigned to three groups (n=25/group); $n{\ddot{a}}ive$, sham, and C2 resection. Three, 7, 10, and 14 days after surgery, cold allodynia was assessed using $20{\mu}L$ of 99.7% acetone. c-Fos and c-Jun were immunohistochemically stained to evaluate activation of dorsal horn gray matter in C2 segments of the spinal cord 2 hours, 1 day, 7 days, and 14 days after surgery. Results : Three days after surgery, the response to acetone in the sham group was significantly greater than in the $n{\ddot{a}}ive$ group, and this significant difference between the $n{\ddot{a}}ive$ and sham groups was maintained throughout the experimental period (p<0.05 at 3, 7, 10, and 14 days). Seven, 10, and 14 days after surgery, the C2 root resection group exhibited a significantly greater response to acetone than the $n{\ddot{a}}ive$ group (p<0.05), and both the sham and C2 resection groups exhibited significantly greater responses to acetone compared with 3 days after surgery. No significant difference in cold allodynia was observed between the sham and C2 root resection groups throughout the experimental period. Two hours after surgery, both the sham and C2 root resection groups exhibited significant increases in c-Fos- and c-Jun-positive neurons compared with the naive group (p=0.0021 and p=0.0358 for the sham group, and p=0.0135 and p=0.014 for the C2 root resection group, respectively). One day after surgery, both the sham and C2 root resection groups exhibited significant decreases in c-Fos -positive neurons compared with two hours after surgery (p=0.0169 and p=0.0123, respectively), and these significant decreases in c-Fos immunoreactivity were maintained in both the sham and C2 root resection groups 7 and 14 days after surgery. The sham and C2 root resection groups presented a tendency toward a decrease in c-Jun-positive neurons 1, 7, and 14 days after surgery, but the decrease did not reach statistical significance. Conclusion : We found no significant difference in cold allodynia and the early expression of c-Fos and c-Jun between the sham and C2 resection groups. Our results may support the routine resection of the C2 nerve root for posterior C1-2 fusion, but, further studies are needed.

Keywords

References

  1. Ahn DK, Lim EJ, Kim BC, Yang GY, Lee MK, Ju JS, et al. : Compression of the trigeminal ganglion produces prolonged nociceptive behavior in rats. Eur J Pain 13 : 568-575, 2009 https://doi.org/10.1016/j.ejpain.2008.07.008
  2. Berrocal YA, Pearse DD, Andrade CM, Hechtman JF, Puentes R, Eaton MJ : Increased spinal c-Fos expression with noxious and non-noxious peripheral stimulation after severe spinal contusion. Neurosci Lett 413 : 58-62, 2007 https://doi.org/10.1016/j.neulet.2006.11.030
  3. Broude E, McAtee M, Kelley MS, Bregman BS : c-Jun expression in adult rat dorsal root ganglion neurons, differential response after central or peripheral axotomy. Exp Neurol 148 : 367-377, 1997 https://doi.org/10.1006/exnr.1997.6665
  4. Campbell JN, Meyer RA : Mechanism of neuropathic pain. Neuron 52 : 77-92, 2006 https://doi.org/10.1016/j.neuron.2006.09.021
  5. Catheline G, Le Guen S, Honore P, Besson JM : Are there long-term changes in the basal or evoked Fos expression in the dorsal horn of the spinal cord of the mononeuropathic rat? Pain 80 : 347-357, 1999 https://doi.org/10.1016/S0304-3959(98)00234-6
  6. Cohen SP, Mao J : Neuropathic pain: mechanisms and their clinical implications. BMJ 348 : f7656, 2014 https://doi.org/10.1136/bmj.f7656
  7. Decosterd I, Woolf CJ : Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 87 : 149-158, 2000 https://doi.org/10.1016/S0304-3959(00)00276-1
  8. Ducati A : Nerves are not made to be cut. World Neurosurg 78 : 601-602, 2012 https://doi.org/10.1016/j.wneu.2011.12.077
  9. Elliott RE, Kang MM, Smith ML, Frempong-Boadu A : C2 nerve root sectioning in posterior atlantoaxial instrumented fusions: a structured review of literature. World Neurosurg 78 : 697-708, 2012 https://doi.org/10.1016/j.wneu.2011.10.035
  10. Elliott RE, Tanweer O, Boah A, Morsi A, Ma T, Smith ML, et al. : Atlantoaxial fusion with screw-rod constructs: meta-analysis and review of literature. World Neurosurg 81 : 411-421, 2014 https://doi.org/10.1016/j.wneu.2012.03.013
  11. Goel A : Treatment of basilar invagination by atlantoaxial joint distraction and direct lateral mass fixation. J Neurosurg Spine 1 : 281-286, 2004 https://doi.org/10.3171/spi.2004.1.3.0281
  12. Goel A : Cervical ganglion 2 (CG2) neurectomy: a window to the atlantoaxial joint. World Neurosurg 78 : 78-79, 2012 https://doi.org/10.1016/j.wneu.2011.08.037
  13. Goel A, Desai KI, Muzumdar DP : Atlantoaxial fixation using plate and screw method: a report of 160 treated patients Neurosurgery 51 : 1351-1356; discussion 1356-1357, 2002 https://doi.org/10.1227/01.NEU.0000309110.78968.F5
  14. Goel A, Laheri V : Plate and screw fixation for atlantoaxial subluxation. Acta Neurochir (Wien) 129 : 47-53, 1994 https://doi.org/10.1007/BF01400872
  15. Hamilton DK, Smith JS, Sansur CA, Dumont AS, Shaffrey CI : C-2 neurectomy during atlantoaxial instrumented fusion in the elderly: patient satisfaction and surgical outcome. J Neurosurg Spine 15 : 3-8, 2011 https://doi.org/10.3171/2011.1.SPINE10417
  16. Harms J, Melcher RP : Posterior C1-C2 fusion with polyaxial screw and rod fixation. Spine (Phila Pa 1976) 26 : 2467-2471, 2001 https://doi.org/10.1097/00007632-200111150-00014
  17. Harris JA : Using c-Fos as a neural marker of pain. Brain Res Bull 45 : 1-8, 1998 https://doi.org/10.1016/S0361-9230(97)00277-3
  18. Jaggi AS, Jain V, Singh N : Animal models of neuropathic pain. Fundam Clin Pharmacol 25 : 1-28, 2011
  19. Jeon HJ, Han SR, Park MK, Yang KY, Bae YC, Ahn DK : A novel trigeminal neuropathic pain model: compression of the trigeminal nerve root produces prolonged nociception in rats. Prog Neuropsychopharmacol Biol Psychiatry 38 : 149-158, 2012 https://doi.org/10.1016/j.pnpbp.2012.03.002
  20. Jeon Y, Kim CE, Jung D, Kwak K, Park S, Lim D, et al. : Curcumin could prevent the development of chronic neuropathic pain in rats with peripheral nerve injury. Curr Ther Res Clin Exp 74 : 1-4, 2013 https://doi.org/10.1016/j.curtheres.2012.10.001
  21. Kang MM, Anderer EG, Elliott RE, Kalhorn SP, Frempong-Boadu A : C2 nerve root sectioning in posterior C1-2 instrumented fusions. World Neurosurg 78 : 170-177, 2012 https://doi.org/10.1016/j.wneu.2011.07.010
  22. Kim IS, Hong JT, Sung JH, Byun JH : Verical reduction using atlantoaxial facet spacer in basilar invagination with atlantoaxial instability. J Korean Neurosurg Soc 50 : 528-531, 2011 https://doi.org/10.3340/jkns.2011.50.6.528
  23. Kim KJ, Yoon YW, Chung JM : Comparison of three rodent neuropathic pain models. Exp Brain Res 113 : 200-206, 1997 https://doi.org/10.1007/BF02450318
  24. Klusakova I, Dubovy P : Experimental models of peripheral neuropathic pain based on traumatic nerve injuries - an anatomical perspective. Ann Anat 191 : 248-259, 2009 https://doi.org/10.1016/j.aanat.2009.02.007
  25. Li H, Li Q, Xie K, Feng S, Wang P, Ma X : Expression of c-Fos and c-Jun in adjacent cervical spinal cord segments following C7 nerve root rhizotomy in rats: indication of a neural pathway between adjacent cervical spinal cord segments. Exp Ther Med 6 : 373-377, 2013 https://doi.org/10.3892/etm.2013.1136
  26. Loukas M, El-Sedfy A, Tubbs RS, Louis RG Jr, Wartmann CT, Curry B, et al. : Identification of greater occipital nerve landmarks for the treatment of occipital neuralgia. Folia Morphol (Warsz) 65 : 337-342, 2006
  27. McCoy ES, Zylka MJ : Enhanced behavioral responses to cold stimuli following CGRP$\alpha$ sensory neuron ablation are dependent on TRPM8. Mol Pain 10 : 69, 2014
  28. Sideris A, Norcini M, Blanck TJ, Reico-Pinto E : Temporal and qualitative differences in the development of allodynic behaviors between mice and rats in a peripheral nerve injury model. Pain Studies and Treatment 2 : 121, 2014 https://doi.org/10.4236/pst.2014.24019
  29. Vanelderen P, Lataster A, Levy R, Mekhail N, van Kleef M, Van Zundert J : Occipital neuralgia. Pain Pract 10 : 137-144, 2010 https://doi.org/10.1111/j.1533-2500.2009.00355.x
  30. Vital JM, Grenier F, Dautheribes M, Baspeyre H, Lavignolle B, Senegas J : An anatomic and dynamic study of the greater occipital nerve (n. of Arnold). Applications to the treatment of Arnold's neuralgia. Surg Radiol Anat 11 : 205-210, 1989 https://doi.org/10.1007/BF02337823
  31. Wang TT, Yuan WL, Ke Q, Song XB, Zhou X, Kang Y, et al. : Effects of electro-acupuncture on the expression of c-jun and c-fos in spared dorsal root ganglion and associated spinal laminae following removal of adjacent dorsal root ganglia in cats. Neuroscience 140 : 1169-1176, 2006 https://doi.org/10.1016/j.neuroscience.2006.03.008
  32. Yeom JS, Buchowski JM, Kim HJ, Chang BS, Lee CK, Riew KD : Postoperative occipital neuralgia with and without C2 nerve root transection during atlantoaxial screw fixation: a post-hoc comparative outcome study of prospectively collected data. Spine J 13 : 786-795, 2013 https://doi.org/10.1016/j.spinee.2013.04.006