Effects and mechanisms of gastric electrical stimulation on visceral pain in a rodent model of gastric hyperalgesia secondary to chemically induced mucosal ulceration

Neurogastroenterology and Motility

Volumn 26, Issue 2, 2014, Pages 176-186

  Sun, Y ^a,b   Tan, Y ^a,c   Song, G ^a   Chen, J D Z ^a,d  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b Paul L Foster School of Medicine   (United States)

^c HAINAN MEDICAL UNIVERSITY   (China)

^d Ningbo Pace Translational Medical Research Center   (China)

Author keywords

Gastric electrical stimulation; Opioid system; Spinal cord; Visceral pain

Indexed keywords

ARTICLE; CAMPYLOBACTER JEJUNI; CLINICAL FEATURE; ENTERITIS; ESCHERICHIA COLI; GASTROINTESTINAL INFECTION; GIARDIA; GIARDIA LAMBLIA; HUMAN; IRRITABLE COLON; NOROVIRUS; PATIENT REFERRAL; POSTINFECTIOUS IRRITABLE BOWEL SYNDROME; PRIORITY JOURNAL; SALMONELLA ENTERICA; SHIGELLA;

GASTRIC ELECTRICAL STIMULATION; OPIOID SYSTEM; SPINAL CORD; VISCERAL PAIN;

ANIMALS; DISEASE MODELS, ANIMAL; ELECTRIC STIMULATION THERAPY; ELECTROMYOGRAPHY; HYPERALGESIA; MALE; RATS; RATS, SPRAGUE-DAWLEY; STOMACH ULCER; VISCERAL PAIN;

EID: 84892679648     PISSN: 13501925     EISSN: 13652982     Source Type: Journal    
DOI: 10.1111/nmo.12248     Document Type: Article

References (55)

1. Kang YM, Lamb K, Gebhart GF, Bielefeldt K. Experimentally induced ulcers and gastric sensory-motor function in rats. Am J Physiol 2005; 288: G284-91.
2. Tack J, Caenepeel P, Fischler B, Piessevaux H, Janssens J. Symptoms associated with hypersensitivity to gastric distention in functional dyspepsia. Gastroenterology 2001; 121: 526-35.
3. Piche M, Arsenault M, Poitras P, Rainville P, Bouin M. Widespread hypersensitivity is related to altered pain inhibition processes in irritable bowel syndrome. Pain 2010; 148: 49-58.
4. Chang L, Munakata J, Mayer EA et al. Perceptual responses in patients with inflammatory and functional bowel disease. Gut 2000; 47: 497-505.
5. Mujica VR, Mudipalli RS, Rao SS. Pathophysiology of chest pain in patients with nutcracker esophagus. Am J Gastroenterol 2001; 96: 1371-7.
6. Schmulson MJ, Mayer EA. Gastrointestinal sensory abnormalities in functional dyspepsia. Baillieres Clin Gastroenterol 1998; 12: 545-56.
7. Verne GN, Robinson ME, Price DD. Hypersensitivity to visceral and cutaneous pain in the irritable bowel syndrome. Pain 2001; 93: 7-14.
8. Mayer EA, Bradesi S, Chang L, Spiegel BM, Bueller JA, Naliboff BD. Functional GI disorders: from animal models to drug development. Gut 2008; 57: 384-404.
9. Dekel R, Drossman DA, Sperber AD. The use of psychotropic drugs in irritable bowel syndrome. Expert Opin Investig Drugs 2013; 22: 329-39.
10. Boyce P, Gilchrist J, Talley NJ, Rose D. Cognitive-behaviour therapy as a treatment for irritable bowel syndrome: a pilot study. Aust N Z J Psychiatry 2000; 34: 300-9.
11. Houghton LA, Cremonini F, Camilleri M et al. Effect of the NK(3) receptor antagonist, talnetant, on rectal sensory function and compliance in healthy humans. Neurogastroenterol Motil 2007; 19: 732-43.
12. Vermeulen W, De Man JG, De Schepper HU et al. Role of TRPV1 and TRPA1 in visceral hypersensitivity to colorectal distension during experimental colitis in rats. Eur J Pharmacol 2013; 698: 404-12.
13. Zhang J, Chen JD. Pacing the gut in motility disorders. Curr Treat Options Gastroenterol 2006; 9: 351-60.
14. Song J, Zhong DX, Qian W, Hou XH, Chen JD. Short pulse gastric electrical stimulation for cisplatin-induced emesis in dogs. Neurogastroenterol Motil 2011; 23: 468-74, e178.
15. Song GQ, Hou X, Yang B, Sun Y, Qian W, Chen JD. A novel method of 2-channel dual-pulse gastric electrical stimulation improves solid gastric emptying in dogs. Surgery 2008; 143: 72-8.
16. Zhang J, Maude-Griffin R, Zhu H et al. Gastric electrical stimulation parameter dependently alters ventral medial hypothalamic activity and feeding in obese rats. Am J Physiol 2011; 301: G912-8.
17. Song GQ, Hou X, Sun Y, Yang B, Qian W, Chen JD. Effects of retrograde gastric electrical stimulation with pulse trains on gastric emptying of solids and plasma hormones in dogs. Am J Surg 2007; 194: 122-7.
18. Lin Z, Forster J, Sarosiek I, McCallum RW. Effect of high-frequency gastric electrical stimulation on gastric myoelectric activity in gastroparetic patients. Neurogastroenterol Motil 2004; 16: 205-12.
19. McCallum RW, Chen JD, Lin Z, Schirmer BD, Williams RD, Ross RA. Gastric pacing improves emptying and symptoms in patients with gastroparesis. Gastroenterology 1998; 114: 456-61.
20. Chen JH, Song GQ, Yin J, Sun Y, Chen JD. Gastric electrical stimulation reduces visceral sensitivity to gastric distention in healthy canines. Auton Neurosci 2011; 160: 16-20.
21. Zhu H, Chen JD. Implantable gastric stimulation inhibits gastric motility via sympathetic pathway in dogs. Obes Surg 2005; 15: 95-100.
22. Xing JH, Chen JD. Effects and mechanisms of long-pulse gastric electrical stimulation on canine gastric tone and accommodation. Neurogastroenterol Motil 2006; 18: 136-43.
23. Qin C, Chen JD, Zhang J, Foreman RD. Modulatory effects and afferent pathways of gastric electrical stimulation on rat thoracic spinal neurons receiving input from the stomach. Neurosci Res 2007; 57: 29-39.
24. Qin C, Sun Y, Chen JD, Foreman RD. Gastric electrical stimulation modulates neuronal activity in nucleus tractus solitarii in rats. Auton Neurosci 2005; 119: 1-8.
25. Sevcik MA, Jonas BM, Lindsay TH et al. Endogenous opioids inhibit early-stage pancreatic pain in a mouse model of pancreatic cancer. Gastroenterology 2006; 131: 900-10.
26. Dunckley P, Wise RG, Fairhurst M et al. A comparison of visceral and somatic pain processing in the human brainstem using functional magnetic resonance imaging. J Neurosci 2005; 25: 7333-41.
27. Friedrich AE, Gebhart GF. Modulation of visceral hyperalgesia by morphine and cholecystokinin from the rat rostroventral medial medulla. Pain 2003; 104: 93-101.
28. Sun Y, Song G, Yin J et al. Effects and mechanisms of electroacupuncture on glucagon-induced small intestinal hypomotility in dogs. Neurogastroenterol Motil 2010; 22: 1217-23, e1318.
29. Tack J, Demedts I, Dehondt G et al. Clinical and pathophysiological characteristics of acute-onset functional dyspepsia. Gastroenterology 2002; 122: 1738-47.
30. Thornley JP, Jenkins D, Neal K, Wright T, Brough J, Spiller RC. Relationship of Campylobacter toxigenicity in vitro to the development of postinfectious irritable bowel syndrome. J Infect Dis 2001; 184: 606-9.
31. Yarushkina N, Bogdanov A, Filaretova L. Somatic pain sensitivity during formation and healing of acetic acid-induced gastric ulcers in conscious rats. Auton Neurosci 2006; 126-127: 100-5.
32. Ozaki N, Bielefeldt K, Sengupta JN, Gebhart GF. Models of gastric hyperalgesia in the rat. Am J Physiol 2002; 283: G666-76.
33. Takagi K, Okabe S, Saziki R. A new method for the production of chronic gastric ulcer in rats and the effect of several drugs on its healing. Jpn J Pharmacol 1969; 19: 418-26.
34. Qin C, Chen JD, Zhang J, Foreman RD. Somatic afferent modulation of thoracic (T9-T10) spinal neurons receiving gastric mechanical input in rats. Neuromodulation 2010; 13: 77-86.
35. Han JS. Acupuncture and endorphins. Neurosci Lett 2004; 361: 258-61.
36. Yin J, Abell TD, McCallum RW, Chen JD. Gastric neuromodulation with Enterra system for nausea and vomiting in patients with gastroparesis. Neuromodulation 2012; 15: 224-31; discussion 231.
37. Zhang J, Chen JD. Systematic review: applications and future of gastric electrical stimulation. Aliment Pharmacol Ther 2006; 24: 991-1002.
38. Liu LS, Winston JH, Shenoy MM, Song GQ, Chen JD, Pasricha PJ. A rat model of chronic gastric sensorimotor dysfunction resulting from transient neonatal gastric irritation. Gastroenterology 2008; 134: 2070-9.
39. Rouzade ML, Fioramonti J, Bueno L. A model for evaluation of gastric sensitivity in awake rats. Neurogastroenterol Motil 1998; 10: 157-63.
40. Li S, Maude-Griffin R, Sun Y, Starkebaum W, Chen JD. Food intake and body weight responses to intermittent vs. continuous gastric electrical stimulation in diet-induced obese rats. Obes Surg 2013; 23: 71-9.
41. Han JS. Acupuncture: neuropeptide release produced by electrical stimulation of different frequencies. Trends Neurosci 2003; 26: 17-22.
42. Oustamanolakis P, Tack J. Dyspepsia: organic versus functional. J Clin Gastroenterol 2012; 46: 175-90.
43. Xu B, Qiao X, Yu X, Liu J. Central opioid peptide-containing neurons mediates therapeutic effect of short-pulse gastric electrical stimulation on dyspepsia-like symptoms in dogs. J Huazhong Univ Sci Technolog Med Sci 2009; 29: 701-4.
44. Ozaki N, Sengupta JN, Gebhart GF. Mechanosensitive properties of gastric vagal afferent fibers in the rat. J Neurophysiol 1999; 82: 2210-20.
45. Ozaki N, Gebhart GF. Characterization of mechanosensitive splanchnic nerve afferent fibers innervating the rat stomach. Am J Physiol 2001; 281: G1449-59.
46. Holzer P, Painsipp E, Schuligoi R. Differential effects of intragastric acid and capsaicin on gastric emptying and afferent input to the rat spinal cord and brainstem. BMC Neurosci 2005; 6: 60.
47. Schicho R, Donnerer J, Liebmann I, Lippe IT. Nociceptive transmitter release in the dorsal spinal cord by capsaicin-sensitive fibers after noxious gastric stimulation. Brain Res 2005; 1039: 108-15.
48. Schuligoi R, Herzeg G, Wachter C, Jocic M, Holzer P. Differential expression of c-fos messenger RNA in the rat spinal cord after mucosal and serosal irritation of the stomach. Neuroscience 1996; 72: 535-44.
49. Peles S, Petersen J, Aviv R et al. Enhancement of antral contractions and vagal afferent signaling with synchronized electrical stimulation. Am J Physiol 2003; 285: G577-85.
50. Qin C, Chen JD, Zhang J, Foreman RD. Characterization of T9-T10 spinal neurons with duodenal input and modulation by gastric electrical stimulation in rats. Brain Res 2007; 1152: 75-86.
51. Koshizaki M, Kawamata M, Shimada SG, Saito Y, Collins JG. 5-HT3 receptors partially mediate halothane depression of spinal dorsal horn sensory neurons. Anesth Analg 2003; 96: 1027-31, table of contents.
52. Greenwood-Van Meerveld B, Johnson AC, Foreman RD, Linderoth B. Attenuation by spinal cord stimulation of a nociceptive reflex generated by colorectal distention in a rat model. Auton Neurosci 2003; 104: 17-24.
53. Krames E, Mousad DG. Spinal cord stimulation reverses pain and diarrheal episodes of irritable bowel syndrome: a case report. Neuromodulation 2004; 7: 82-8.
54. Liu S, Peng S, Hou X, Ke M, Chen JD. Transcutaneous electroacupuncture improves dyspeptic symptoms and increases high frequency heart rate variability in patients with functional dyspepsia. Neurogastroenterol Motil 2008; 20: 1204-11.
55. Xu GY, Winston JH, Chen JD. Electroacupuncture attenuates visceral hyperalgesia and inhibits the enhanced excitability of colon specific sensory neurons in a rat model of irritable bowel syndrome. Neurogastroenterol Motil 2009; 21: 1302-e125.