PAIN
Volume 139, Issue 3 , Pages 520-532 , 31 October 2008

A new rat model for thrombus-induced ischemic pain (TIIP); development of bilateral mechanical allodynia

  • Hyoung-Sig Seo

      Affiliations

    • Department of Veterinary Physiology, College of Veterinary Medicine and BK21 program for Veterinary Science, Seoul National University, San 56-1, Sillim-dong, Gwanak-gu, Seoul, South Korea
    • These authors contributed equally to this study.
  • ,
  • Hyun-Woo Kim

      Affiliations

    • Department of Physiology, College of Medicine and Research Institute for Medical Sciences, Chungnam National University, Daejeon, South Korea
    • These authors contributed equally to this study.
  • ,
  • Dae-Hyun Roh

      Affiliations

    • Department of Veterinary Physiology, College of Veterinary Medicine and BK21 program for Veterinary Science, Seoul National University, San 56-1, Sillim-dong, Gwanak-gu, Seoul, South Korea
  • ,
  • Seo-Yeon Yoon

      Affiliations

    • Department of Veterinary Physiology, College of Veterinary Medicine and BK21 program for Veterinary Science, Seoul National University, San 56-1, Sillim-dong, Gwanak-gu, Seoul, South Korea
  • ,
  • Young-Bae Kwon

      Affiliations

    • Department of Pharmacology, Institute for Medical Science, Chonbuk National University Medical School, Jeonju, South Korea
  • ,
  • Ho-Jae Han

      Affiliations

    • Department of Veterinary Physiology, College of Veterinary Medicine and Biotherapy Human Resources Center, Chonnam National University, Gwangju, South Korea
  • ,
  • Jin Mo Chung

      Affiliations

    • Department of Neuroscience and Cell Biology, University of Texas Medical Branch, 301 University Boulevard, Galveston, TX 77555-1069, USA
  • ,
  • Alvin J. Beitz

      Affiliations

    • Department of Veterinary and Biomedical Sciences, College of Veterinary Medicine, University of Minnesota, St. Paul, MN 55108, USA
  • ,
  • Jang-Hern Lee

      Affiliations

    • Department of Veterinary Physiology, College of Veterinary Medicine and BK21 program for Veterinary Science, Seoul National University, San 56-1, Sillim-dong, Gwanak-gu, Seoul, South Korea
    • Corresponding Author InformationCorresponding author. Tel.: +82 2 880 1272; fax: +82 2 885 2732.

Received 11 January 2008 ,Revised 3 May 2008 ,Accepted 2 June 2008.

References 

  1. Balonov K, Khodorova A, Strichartz GR. Tactile allodynia initiated by local subcutaneous endothelin-1 is prolonged by activation of TRPV-1 receptors. Exp Biol Med (Maywood). 2006;231:1165–1170
  2. Bedarida GV, Hoffmann U, Tato F. Acute lower limb ischemia due to thrombo-embolic arterial occlusions in two previously healthy men with markedly elevated Lp(a). Vasc Med. 2006;11:259–262
  3. Blinc A, Poredos P. Pharmacological prevention of atherothrombotic events in patients with peripheral arterial disease. Eur J Clin Invest. 2007;37:157–164
  4. Cho J, Seo H, Yun C, Koo B, Yoshida S, Koga T, et al. In vitro and in vivo studies of AT-1362, a newly synthesized and orally active inhibitor of thrombin. Thromb Res. 2000;100:97–107
  5. Choksy S, Pockley AG, Wajeh YE, Chan P. VEGF and VEGF receptor expression in human chronic critical limb ischaemia. Eur J Vasc Endovasc Surg. 2004;28:660–669
  6. Coderre TJ, Xanthos DN, Francis L, Bennett GJ. Chronic post-ischemia pain (CPIP): a novel animal model of complex regional pain syndrome-type I (CRPS-I; reflex sympathetic dystrophy) produced by prolonged hindpaw ischemia and reperfusion in the rat. Pain. 2004;112:94–105
  7. Dashwood MR, Tsui JC. The effect of acute ischemia on ET-1 and its receptors in patients with underlying chronic ischemia of the lower limb. Exp Biol Med (Maywood). 2006;231:802–805
  8. Dawson DL, Mills JL. Critical limb ischemia. Curr Treat Options Cardiovasc Med. 2007;9:159–170
  9. De-Melo JD, Tonussi CR, D’Orleans-Juste P, Rae GA. Effects of endothelin-1 on inflammatory incapacitation of the rat knee joint. J Cardiovasc Pharmacol. 1998;31 Suppl. 1:S518–S520
  10. Duprez DA. Pharmacological interventions for peripheral artery disease. Expert Opin Pharmacother. 2007;8:1465–1477
  11. England JD, Ferguson MA, Hiatt WR, Regensteiner JG. Progression of neuropathy in peripheral arterial disease. Muscle Nerve. 1995;18:380–387
  12. Forsythe JA, Jiang BH, Iyer NV, Agani F, Leung SW, Koos RD, et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol. 1996;16:4604–4613
  13. Fry DL. Arotic Evans blue dye accumulation: its measurement and interpretation. Am J Physiol. 1977;232:H204–H222
  14. Garrison CJ, Dougherty PM, Kajander KC, Carlton SM. Staining of glial fibrillary acidic protein (GFAP) in lumbar spinal cord increases following a sciatic nerve constriction injury. Brain Res. 1991;565:1–7
  15. Gokin AP, Fareed MU, Pan HL, Hans G, Strichartz GR, Davar G. Local injection of endothelin-1 produces pain-like behavior and excitation of nociceptors in rats. J Neurosci. 2001;21:5358–5366
  16. Hargreaves K, Dubner R, Brown F, Flores C, Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain. 1988;32:77–88
  17. Ho TK, Rajkumar V, Ponticos M, Leoni P, Black DC, Abraham DJ, et al. Increased endogenous angiogenic response and hypoxia-inducible factor-1alpha in human critical limb ischemia. J Vasc Surg. 2006;43:125–133
  18. Hylden JL, Wilcox GL. Intrathecal morphine in mice: a new technique. Eur J Pharmacol. 1980;67:313–316
  19. Koltzenburg M, Wall PD, McMahon SB. Does the right side know what the left is doing?. Trends Neurosci. 1999;22:122–127
  20. Kurz KD, Main BW, Sandusky GE. Rat model of arterial thrombosis induced by ferric chloride. Thromb Res. 1990;60:269–280
  21. Kwon YB, Lee JD, Lee HJ, Han HJ, Mar WC, Kang SK, et al. Bee venom injection into an acupuncture point reduces arthritis associated edema and nociceptive responses. Pain. 2001;90:271–280
  22. Laghi Pasini F, Pastorelli M, Beermann U, de Candia S, Gallo S, Blardi P, et al. Peripheral neuropathy associated with ischemic vascular disease of the lower limbs. Angiology. 1996;47:569–577
  23. Lang PM, Schober GM, Rolke R, Wagner S, Hilge R, Offenbacher M, et al. Sensory neuropathy and signs of central sensitization in patients with peripheral arterial disease. Pain. 2006;124:190–200
  24. Ludwig J, Gorodetskaya N, Schattschneider J, Janig W, Baron R. Behavioral and sensory changes after direct ischemia-reperfusion injury in rats. Eur J Pain. 2007;11:677–684
  25. Meru AV, Mittra S, Thyagarajan B, Chugh A. Intermittent claudication: an overview. Atherosclerosis. 2006;187:221–237
  26. Milligan ED, Twining C, Chacur M, Biedenkapp J, O’Connor K, Poole S, et al. Spinal glia and proinflammatory cytokines mediate mirror–image neuropathic pain in rats. J Neurosci. 2003;23:1026–1040
  27. Morimoto S, Cassell MD, Beltz TG, Johnson AK, Davisson RL, Sigmund CD. Elevated blood pressure in transgenic mice with brain-specific expression of human angiotensinogen driven by the glial fibrillary acidic protein promoter. Circ Res. 2001;89:365–372
  28. Nicholson CD. Experimental models of chronic lower extremity arterial occlusive disease: lessons for drug development. Vasc Med. 1996;1:43–49
  29. Patterson CE, Rhoades RA, Garcia JG. Evans blue dye as a marker of albumin clearance in cultured endothelial monolayer and isolated lung. J Appl Physiol. 1992;72:865–873
  30. Piao ZG, Cho IH, Park CK, Hong JP, Choi SY, Lee SJ, et al. Activation of glia and microglial p38 MAPK in medullary dorsal horn contributes to tactile hypersensitivity following trigeminal sensory nerve injury. Pain. 2006;121:219–231
  31. Pinel C, Wice SM, Hiebert LM. Orally administered heparins prevent arterial thrombosis in a rat model. Thromb Haemost. 2004;91:919–926
  32. Raghavendra V, Tanga FY, DeLeo JA. Complete Freunds adjuvant-induced peripheral inflammation evokes glial activation and proinflammatory cytokine expression in the CNS. Eur J Neurosci. 2004;20:467–473
  33. Roh DH, Kwon YB, Kim HW, Ham TW, Yoon SY, Kang SY, et al. Acupoint stimulation with diluted bee venom (apipuncture) alleviates thermal hyperalgesia in a rodent neuropathic pain model: involvement of spinal alpha 2-adrenoceptors. J Pain. 2004;5:297–303
  34. Semenza GL, Agani F, Feldser D, Iyer N, Kotch L, Laughner E, et al. Hypoxia, HIF-1, and the pathophysiology of common human diseases. Adv Exp Med Biol. 2000;475:123–130
  35. Spataro LE, Sloane EM, Milligan ED, Wieseler-Frank J, Schoeniger D, Jekich BM, et al. Spinal gap junctions: potential involvement in pain facilitation. J Pain. 2004;5:392–405
  36. St-Pierre P, Bouffard L, Papirakis ME, Maheux P. Increased extravasation of macromolecules in skeletal muscles of the Zucker rat model. Obesity (Silver Spring). 2006;14:787–793
  37. Tuomisto TT, Rissanen TT, Vajanto I, Korkeela A, Rutanen J, Yla-Herttuala S. HIF-VEGF-VEGFR-2, TNF-alpha and IGF pathways are upregulated in critical human skeletal muscle ischemia as studied with DNA array. Atherosclerosis. 2004;174:111–120
  38. Wieseler-Frank J, Maier SF, Watkins LR. Glial activation and pathological pain. Neurochem Int. 2004;45:389–395
  39. Woolf CJ, Wall PD. Relative effectiveness of C primary afferent fibers of different origins in evoking a prolonged facilitation of the flexor reflex in the rat. J Neurosci. 1986;6:1433–1442
  40. Zhang ET, Ossipov MH, Zhang DQ, Lai J, Porreca F. Nerve injury-induced tactile allodynia is present in the absence of FOS labeling in retrogradely labeled post-synaptic dorsal column neurons. Pain. 2007;129:143–154

PII: S0304-3959(08)00298-4

doi: 10.1016/j.pain.2008.06.011

PAIN
Volume 139, Issue 3 , Pages 520-532 , 31 October 2008