Review article: Gastric electrical stimulation for gastroparesis - Physiological foundations, technical aspects and clinical implications

Alimentary Pharmacology and Therapeutics

Volumn 30, Issue 7, 2009, Pages 681-694

  Soffer, E ^a,g   Abell, T ^b   Lin, Z ^c   Lorincz, A ^d   McCallum, R ^c   Parkman, H ^e   Policker, S ^f   Ordog, T ^d  

^a CEDARS SINAI MEDICAL CENTER   (United States)

^b UNIVERSITY OF MISSISSIPPI SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^d MAYO CLINIC   (United States)

^e TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f MetaCure (USA) Inc   (United States)

^g Center for Digestive Diseases   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CLINICAL TRIAL; ELECTRIC ACTIVITY; ELECTROSTIMULATION THERAPY; HUMAN; NONHUMAN; NUTRITIONAL STATUS; PRIORITY JOURNAL; QUALITY OF LIFE; REVIEW; SENSORY NERVE CONDUCTION; STOMACH EMPTYING; STOMACH MOTILITY; STOMACH PARESIS; SYSTEMATIC REVIEW;

ELECTRIC STIMULATION THERAPY; EPIDEMIOLOGIC METHODS; GASTRIC EMPTYING; GASTROPARESIS; HUMANS; TREATMENT OUTCOME;

EID: 69949166902     PISSN: 02692813     EISSN: 13652036     Source Type: Journal    
DOI: 10.1111/j.1365-2036.2009.04082.x     Document Type: Review

References (100)

1. Kelly KA, La Force RC. Pacing the canine stomach with electrical stimulation. Am J Physiol 1972 222 : 588 594.
2. Lin ZY, McCallum RW, Schirmer BD, et al. Effects of pacing parameters in the entrainment of gastric slow waves in patients with gastroparesis. Am J Physiol 1998 274 : G186 91.
3. Eagon JC, Kelly KA. Effects of gastric pacing on canine gastric motility and emptying. Am J Physiol 1993 265 : G767 74.
4. McCallum RW, Chen JDZ, Lin ZY, et al. Gastric pacing improves gastric emptying and symptoms in patients with gastroparesis. Gastroenterology 1998 114 : 456 461.
5. Hocking MP, Vogel SB, Sninsky CA. Human gastric myoelectrical activity and gastric emptying following gastric surgery and with pacing. Gastroenterology 1992 103 : 1811 1816.
6. Miedema BW, Sarr MG, Kelly KA. Pacing the human stomach. Surgery 1992 111 : 143 150.
7. Huizinga JD. Gastrointestinal peristalsis: joint action of enteric nerves, smooth muscle, and interstitial cells of Cajal. Microsc Res Tech 1999 47 : 239 247.
8. Sanders KM. Regulation of smooth muscle excitation and contraction. Neurogastroenterol Motil 2008 20 (Suppl. 1 39 53.
9. Furness JB. The enteric nervous system: normal functions and enteric neuropathies. Neurogastroenterol Motil 2008 20 (Suppl. 1 32 8.
10. Farrugia G. Interstitial cells of Cajal in health and disease. Neurogastroenterol Motil 2008 20 (Suppl. 1 54 63.
11. Sanders KM, Koh SD, Ward SM. Interstitial cells of Cajal as pacemakers in the gastrointestinal tract. Annu Rev Physiol 2006 68 : 307 343.
12. Ward SM, Sanders KM. Involvement of intramuscular interstitial cells of Cajal in neuroeffector transmission in the gastrointestinal tract. J Physiol 2006 576 : 675 682.
13. Huizinga JD, Liu LW, Fitzpatrick A, et al. Deficiency of intramuscular ICC increases fundic muscle excitability but does not impede nitrergic innervation. Am J Physiol Gastrointest Liver Physiol 2008 294 : G589 94.
14. Sergeant GP, Large RJ, Beckett EA, et al. Microarray comparison of normal and W/Wv mice in the gastric fundus indicates a supersensitive phenotype. Physiol Genomics 2002 11 : 1 9.
15. Szurszewski JH. A migrating electric complex of canine small intestine. Am J Physiol 1969 217 : 1757 1763.
16. Ward SM, Burns AJ, Torihashi S, et al. Impaired development of interstitial cells and intestinal electrical rhythmicity in steel mutants. Am J Physiol 1995 269 : C1577 85.
17. Alberti E, Mikkelsen HB, Wang XY, et al. Pacemaker activity and inhibitory neurotransmission in the colon of Ws/Ws mutant rats. Am J Physiol Gastrointest Liver Physiol 2007 292 : G1499 510.
18. Maeda H, Yamagata A, Nishikawa S, et al. Requirement of c-kit for development of intestinal pacemaker system. Development 1992 116 : 369 375.
19. Rich A, Leddon SA, Hess SL, et al. Kit-like immunoreactivity in the zebrafish gastrointestinal tract reveals putative ICC. Dev Dyn 2007 236 : 903 911.
20. Komuro T. Structure and organization of interstitial cells of Cajal in the gastrointestinal tract. J Physiol 2006 576 : 653 658.
21. Rich A, Miller SM, Gibbons SJ, et al. Local presentation of Steel factor increases expression of c-kit immunoreactive interstitial cells of Cajal in culture. Am J Physiol Gastrointest Liver Physiol 2003 284 : G313 20.
22. Lorincz A, Redelman D, Horvath VJ, et al. Progenitors of interstitial cells of Cajal in the postnatal murine stomach. Gastroenterology 2008 134 : 1083 1093.
23. Hirst GD, Edwards FR. Electrical events underlying organized myogenic contractions of the guinea pig stomach. J Physiol 2006 576 : 659 665.
24. Sivarao DV, Mashimo H, Goyal RK. Pyloric sphincter dysfunction in NOS-/- and W/Wv mutant mice: animal models of gastroparesis and duodenogastric reflux. Gastroenterology 2008 135 : 1258 1266.
25. Forrest AS, Ordog T, Sanders KM. Neural regulation of slow-wave frequency in the murine gastric antrum. Am J Physiol Gastrointest Liver Physiol 2006 290 : G486 9.
26. Beckett EA, McGeough CA, Sanders KM, et al. Pacing of interstitial cells of Cajal in the murine gastric antrum: neurally mediated and direct stimulation. J Physiol 2003 553 : 545 559.
27. Fox EA, Phillips RJ, Byerly MS, et al. Selective loss of vagal intramuscular mechanoreceptors in mice mutant for steel factor, the c-Kit receptor ligand. Anat Embryol (Berl) 2002 205 : 325 342.
28. Kraichely RE, Farrugia G. Mechanosensitive ion channels in interstitial cells of Cajal and smooth muscle of the gastrointestinal tract. Neurogastroenterol Motil 2007 19 : 245 252.
29. Streutker CJ, Huizinga JD, Driman DK, et al. Interstitial cells of Cajal in health and disease. Part I: normal ICC structure and function with associated motility disorders. Histopathology 2007 50 : 176 189.
30. Ordog T. Interstitial cells of Cajal in diabetic gastroenteropathy. Neurogastroenterol Motil 2008 20 : 8 18.
31. Lee HT, Hennig GW, Fleming NW, et al. The mechanism and spread of pacemaker activity through myenteric interstitial cells of Cajal in human small intestine. Gastroenterology 2007 132 : 1852 1865.
32. Wang B, Kunze WA, Zhu Y, et al. In situ recording from gut pacemaker cells. Pflugers; Arch - Eur J Physiol 2008 457 : 243 251.
33. Ward SM, Ordog T, Koh SD, et al. Pacemaking in interstitial cells of Cajal depends upon calcium handling by endoplasmic reticulum and mitochondria. J Physiol 2000 525 : 355 361.
34. 2+ currents are necessary for slow-wave propagation in the canine gastric antrum. Am J Physiol Cell Physiol 2007 293 : C1645 59.
35. Ordog T, Baldo M, Danko R, et al. Plasticity of electrical pacemaking by interstitial cells of Cajal and gastric dysrhythmias in W/W mutant mice. Gastroenterology 2002 123 : 2028 2040.
36. Lee HT, Hennig GW, Fleming NW, et al. Septal interstitial cells of Cajal conduct pacemaker activity to excite muscle bundles in human jejunum. Gastroenterology 2007 133 : 907 917.
37. Walter GC, Phillips RJ, Baronowsky EA, Powley TL. Versatile, high-resolution anterograde labeling of vagal efferent projections with dextran amines. J Neurosci Methods 2009 178 : 1 9.
38. Beckett EA, Takeda Y, Yanase H, et al. Synaptic specializations exist between enteric motor nerves and interstitial cells of Cajal in the murine stomach. J Comp Neurol 2005 493 : 193 206.
39. Ordog T, Redelman D, Horowitz NN, et al. Immunomagnetic enrichment of interstitial cells of Cajal. Am J Physiol Gastrointest Liver Physiol 2004 286 : G351 60.
40. Sanders KM, Ordog T, Koh SD, et al. Development and plasticity of interstitial cells of Cajal. Neurogastroenterol Motil 1999 11 : 311 338.
41. Huizinga JD, Lammers WJ. Gut peristalsis is governed by a multitude of cooperating mechanisms. Am J Physiol Gastrointest Liver Physiol 2009 296 : G1 8.
42. Lammers WJ, Ver Donck L, Stephen B, et al. Origin and propagation of the slow wave in the canine stomach: the outlines of a gastric conduction system. Am J Physiol Gastrointest Liver Physiol 2009 96 : 1200 1210.
43. Mintchev MP, Sanmiguel CP, Amaris M, et al. Microprocessor-controlled movement of solid gastric content using sequential neural electrical stimulation. Gastroenterology 2000 118 : 258 263.
44. Watkins CC, Sawa A, Jaffrey S, et al. Insulin restores neuronal nitric oxide synthase expression and function that is lost in diabetic gastropathy. J Clin Invest 2000 106 : 373 384.
45. Prutchi D, Norris M. Design and Development of Medical Electronic Instrumentation: A Practical Perspective of the Design, Construction, and Test of Medical Devices. Wiley-Interscience, Hoboken, NJ, USA, 2004.
46. Merril DR, Bikson M, Jefferys JGR. Electrical stimulation of excitable tissue: design of efficacious and safe protocols. J of Neuroscience Methods 2005 141 : 171 198.
47. Weiland JD, Anderson DJ, Humayun MS. In vitro electrical properties for iridium oxide versus titanium nitride stimulating electrodes. IEEE Trans Biomed Eng 2002 49 : 1574 1579.
48. Cogan SF, Troyk PR, Ehrlich J, et al. Potential-biased, asymmetric waveforms for charge-injection with activated iridium oxide (AIROF) neural stimulation electrodes. IEEE Trans Biomed Eng 2006 53 : 327 332.
49. Bilgutay AM, Wingrove R, Grifen WO, et al. Gastro-intestinal pacing: a new concept in the treatment of ileus. Ann Surg 1963 158 : 338 348.
50. Quast DC, Beall AC, DeBakey ME. Clinical evaluation of the gastrointestinal pacer. Surg Gyn Obs 1965 120 : 35 7.
51. Berger T, Kewenter J, Kock NG. Response to gastrointestinal pacing: antral, duodenal and jejunal motility in control and postoperative patients. Ann Surg 1966 164 : 139 144.
52. Sarna SK, Daniel EE. Gastrointestinal electrical activity: terminology. Gastroenterology 1975 68 : 1631 1635.
53. Hinder RA, Kelly KA. Human gastric pacemaker potential: site of origin, spread, and response to gastric transaction and proximal gastric vagotomy. Am J Surg 1977 133 : 29 33.
54. Sarna SK, Bowes KL, Daniel EE. Gastric pacemakers. Gastroenterology 1976 70 : 226 231.
55. Bellahsène B-E, Schirmer BD, Updike OL, et al. Effect of electrical stimulation on gastric emptying. Dig Dis Sci 1987 32 : 902.
56. Bellahsène B-E, Lind CD, Schirmer BD, et al. Acceleration of gastric emptying with electrical stimulation in a canine model of gastroparesis. Am J Physiol 1992 262 : G826 34.
57. Familoni BO, Abell TL, Nemoto D, et al. Efficacy of electrical stimulation at frequencies higher than basal rate in canine stomach. Dig Dis Sci 1997 42 : 892 897.
58. Familoni BO, Abell TL, Voeller G, et al. Electrical stimulation at a frequency higher than basal rate in human stomach. Dig Dis Sci 1997 42 : 885.
59. Brody F, Vaziri K, Saddler A, et al. Gastric electrical stimulation for gastroparesis. J Am Coll Surg 2008 207 : 533 538.
60. Al-Jubury A, Granger S, Barnes J, et al. Laparoscopy shortens the length of stay in patients with gastric electrical stimulation. J Soc Laparoendo Surg 2005 9 : 305 310.
61. Curuchi AP, Al-Juburi A, Familoni B, et al. Gastric electrical stimulation-a ten year experience. Gastroenterology 2004 126 : A1284.
62. Abell T, Lou J, Tabbaa M, et al. Gastric electrical stimulation for gastroparesis improves nutritional parameters at short, intermediate, and long-term follow-up. JPEN 2003 27 : 277 281.
63. Anand C, Al-Juburi A, Familoni B, et al. Gastric electrical stimulation is safe and effective: a long-term study in patients with drug-refractory gastroparesis in three regional centers. Digestion 2007 75 : 83 9.
64. Abell T, McCallum R, Hocking M, et al. Gastric electrical stimulation for medically refractory gastroparesis. Gastroenterology 2003 125 : 421 428. (Pubitemid 36929423)
65. Forester J, Sarosiek I, Lin Z, et al. Further experience with gastric stimulation to treat drug refractory gastroparesis. Am J Gastroenterol 2003 186 : 690 695.
66. Lin Z, Sarosiek I, Forster J, et al. Symptom responses, long-term outcomes and adverse events beyond 3 years of high-frequency gastric electrical stimulation for gastroparesis. Neurogastornterol Motil 2006 18 : 18 27.
67. Cutts T, Luo J, Starkebaum W, et al. Is gastric electrical stimulation is superior to standard pharmacologic therapy in improving GI symptoms, healthcare resources, and long-term health care costs? Neurogastroenterol Motil 2005 17 : 35 43.
68. Lin Z, McElhinney C, Sarosiek I, et al. Chronic gastric electrical stimulation for gastroparesis reduces the use of prokinetic and/or antiemetic medications and the need for hospitalizations. Dig Dis Sci 2005 50 : 1328 1334.
69. Maranki JL, Lytes V, Meilahn JE, et al. Predictive factors for clinical improvement with Enterra gastric electric stimulation treatment for refractory gastroparesis. Dig Dis Sci 2008 53 : 2072 2078.
70. Forster J, Damjanov I, Lin Z, et al. Absence of the interstitial cells of Cajal in patients with gastroparesis and correlation with clinical findings. J Gastrointest Surg 2005 9 : 102 108.
71. Chen JDZ, Qian L, Ouyang H, et al. Gastric electrical stimulation with short pulses reduces vomiting but not dysrhythmia in dogs. Gastroenterolgy 2003 124 : 401 409.
72. Lin Z, Forster J, Sarosiek I, et al. Effect of high-frequency gastric electrical stimulation on gastric myoeleftrical activity in gastroparetic patients. Neurogastroenterol Motil 2004 16 : 205 212.
73. Abell T, Custem EV, Abrahamsson H, et al. Gastric electrical stimulation in intractable symptomatic gastroparesis. Digestion 2002 66 : 204 221.
74. Lin Z, Forster J, Sarosiek I, et al. Treatment of gastroparesis by high-frequency gastric electrical stimulation. Diabetes Care 2004 27 : 1071 1076.
75. Lin Z, Hou Q, Sarosiek I, et al. Association between changes in symptoms and gastric emptying in gastroparetic patients treated with gastric electrical stimulation. Neurogastroenterol Motil 2008 20 : 464 470.
76. Van der Voort IR, Becker JC, Dietl KH, et al. Gastric electrical stimulation results in improved metabolic control in diabetic patients suffering from gastroparesis. Exp Clin Endocrinol Diab 2005 113 : 38 42.
77. Bityutskiy LP, Soykan I, McCallum RW. Viral astroparesis; a subgroup of idiopathic gastroparesis-clinical characteristics and long-term outcomes. Am J Gastroenterol 1997 92 : 1501 1504.
78. Horowitz M, Harding PE, Maddox AF, et al. Gastric and esophageal emptying in patients with type 2 (non insulin-dependent) diabetes mellitus. Diabetologia 1989 32 : 151 159.
79. Xing JH, Brody F, Brodsky J, et al. Gastric electrical stimulation at proximal stomach induces gastric relaxation in dogs. Neurogastroenterol Motil 2003 15 : 15 23.
80. Xing JH, Chen JDZ. Gastric electrical stimulation with parameters of gastroparesis enhances gastric accommodation and alleviates distension-induced symptoms in dogs. Dig Dis Sci 2006 51 : 2160 2164.
81. Tack J, Piessevaux H, Coulie B, et al. Role of impaired gastric accommodation to a meal in functional dyspepsia. Gastroenterology 1998 115 : 1346 1352.
82. Samson M, Roelfus JM, Akkermans LM, et al. Proximal gastric motor activity in response to a liquid meal in type 1 diabetes mellitus with autonomic neuropathy. Dig Dis Sci 1998 43 : 491 496.
83. McCallum RW, Lin Z, Wetzl P, et al. Clinical response to gastric electrical stimulation in patients with postsurgical gastroparesis. Clin Gastroenterol Hepatol 2005 3 : 49 54.
84. Oubre B, Luo J, Al-Juburi A, et al. Pilot study on gastric electrical stimulation on surgery-associated gastroparesis: long-term outcome. South Med J 2005 98 : 693 697.
85. Salameh J, Schmieg RE, Runnels JM, et al. Refractory gastroparesis after roux-en-y gastric bypass: surgical treatment with implantable pacemaker. J Gastrointest Surg 2007 11 : 1669 1672.
86. Qin C, Sun Y, Chen JD, Foreman RD. Gastric electrical stimulation modulates neuronal activity in nucleus tractus solitarius in rats. Auton Neurosci 2005 119 : 1 8. (Pubitemid 40704694)
87. McCallum RW, Dusing RW, Sarosiek I, et al. Mechanisms of high-frequency electrical stimulation in the stomach in gastroparetic patients. Conf Proc and Int Conf IEEE Eng Med Biol Soc 2006 1 : 5400 5540.
88. Luo J, Al-Juburi A, Rashed H, et al. Gastric electrical stimulation is associated with improvement in pancreatic exocrine function. Pancreas 2004 29 : e41 4.
89. Andersson S, lonroth H, Simren M, et al. Gastric electrical stimulation for intractable vomiting in patients with chronic intestinal pseudiobstruction. Neurogastroenterol Motil 2006 18 : 823 830.
90. Filichia LA, Cendan JC. Small case series of gastric electrical stimulation for the management of transplant-induced gastroparesis. J Surg Res 2008 148 : 90 3.
91. Gourcerol G, Leblanc I, Leroi AM, et al. Gastric electrical stimulation in medically refractory nausea and vomiting. Eur J Gastroenterol Hepatol 2007 19 : 29 35.
92. Islam S, Vick LR, Runnels MJ, et al. Gastric electrical stimulation for children with intractable nausea and gastroparesis. J Pediatr Surg 2008 43 : 437 442.
93. Matzel KE, Kamm MA, Stosser M, et al. Sacral spinal nerve stimulation for fecal incontinence: multicenter study. Lancet 2004 363 : 1270 1276.
94. Ayinala S, Bastita O, Al-Juburi A, et al. Temporary gastric electrical stimulation can be safely performed with oral or PEG placed electrodes in patients with drug refractory gastroparesis. Gastrointest Endosc 2005 61 : 455 461.
95. Abidi N, Starkebaum WL, Abell TL. An energy algorithm improves symptoms in some patients with gastroparesis and treated with gastric electrical stimulation. Neurogastroenterol Motil 2006 18 : 334 338.
96. Chen JD, Xu X, Zhang J, et al. Efficiency and efficacy of multi-channel gastric electrical stimulation. Neuogastroenterol Motil 2005 17 : 878 882.
97. Song G, Hou X, Yang B, et al. Two-channel gastric electrical stimulation accelerates delayed gastric emptying induced by vasopressin. Dig Dis Sci 2005 50 : 662 668.
98. Sarosiek I, Forester J, Roeser k, et al. Effect of multi-point gastric electrical pacing (MGP) on symptoms, gastric emptying and electrical activity in diabetic gastroparesis. Gastroenterology 2008 134 : A847.
99. Mason RJ, Lipham J, Eckerling G, et al. Gastric electrical stimulation: an alternative surgical therapy for patients with gastroparesis. Arch Surg 2005 140 : 841 848.
100. McKenna D, Beverstein G, Reichelderfer M, et al. Gastric electrical stimulation is an effective and safe treatment for medically refractory gastroparesis. Surgery 2008 144 : 566 574.