Advertisement

Gastroparesis pp 177-190 | Cite as

Diabetic Gastroparesis

  • Christopher K. RaynerEmail author
  • Karen L. Jones
  • Michael Horowitz
Chapter
Part of the Clinical Gastroenterology book series (CG)

Abstract

Gastric emptying is frequently disordered in patients with long-standing type 1 and type 2 diabetes mellitus. While patients with diabetes present with similar symptoms to those with idiopathic gastroparesis, the relationship between gastric emptying and glycemic control represents an important additional consideration in the diabetic group. Specifically, acute variations in the blood glucose concentration affect the rate of gastric emptying, while conversely, gastric emptying is a key determinant of postprandial blood glucose. This has implications both for how gastroparesis should be defined in patients with diabetes, and for its optimal management.

Keywords

Diabetes mellitus Interstitial cells of Cajal Nitric oxide Heme ­oxygenase 1 Incretin Glucagon-like peptide 1 Insulin Blood glucose concentration 

References

  1. 1.
    Kassander P. Asymptomatic gastric retention in diabetics (gastroparesis diabeticorum). Gastroenterology. 1958;48:797–812.Google Scholar
  2. 2.
    Soykan I, Sivri B, Sarosiek I, et al. Demography, clinical characteristics, psychological and abuse profiles, treatment, and long-term follow-up of patients with gastroparesis. Dig Dis Sci. 1998;43:2398–404.PubMedCrossRefGoogle Scholar
  3. 3.
    Horowitz M, Maddox AF, Wishart JM, et al. Relationships between oesophageal transit and solid and liquid gastric emptying in diabetes mellitus. Eur J Nucl Med. 1991;18:229–34.PubMedCrossRefGoogle Scholar
  4. 4.
    Jones KL, Russo A, Stevens JE, et al. Predictors of delayed gastric emptying in diabetes. Diabetes Care. 2001;24:1264–9.PubMedCrossRefGoogle Scholar
  5. 5.
    Frank JW, Saslow SB, Camilleri M, et al. Mechanism of accelerated gastric emptying of liquids and hyperglycemia in patients with type II diabetes mellitus. Gastroenterology. 1995;109:755–65.PubMedCrossRefGoogle Scholar
  6. 6.
    Jones KL, Horowitz M, Carney BI, et al. Gastric emptying in early noninsulin-dependent diabetes mellitus. J Nucl Med. 1996;37:1643–8.PubMedGoogle Scholar
  7. 7.
    Lipp RW, Schnedl WJ, Hammer HF, et al. Evidence of accelerated gastric emptying in longstanding diabetic patients after ingestion of a semisolid meal. J Nucl Med. 1997;38:814–8.PubMedGoogle Scholar
  8. 8.
    Hejazi RA, Patil H, McCallum RW. Dumping syndrome: establishing criteria for diagnosis and identifying new etiologies. Dig Dis Sci. 2010;55:117–23.PubMedCrossRefGoogle Scholar
  9. 9.
    Kuo P, Stevens JE, Bellon M, et al. Acute effects of pancreatic enzyme replacement on gastric emptying and postprandial glycaemia in patients with cystic fibrosis (abstract). Gastroenterology. 2009;136(5 Suppl 1):P-272.Google Scholar
  10. 10.
    Bytzer P, Talley NJ, Leemon M, et al. Prevalence of gastrointestinal symptoms associated with diabetes mellitus: a population-based survey of 15,000 adults. Arch Intern Med. 2001;161:1989–96.PubMedCrossRefGoogle Scholar
  11. 11.
    Samsom M, Vermeijden JR, Smout AJ, et al. Prevalence of delayed gastric emptying in diabetic patients and relationship to dyspeptic symptoms: a prospective study in unselected diabetic patients. Diabetes Care. 2003;26:3116–22.PubMedCrossRefGoogle Scholar
  12. 12.
    Bharucha AE, Camilleri M, Forstrom LA, et al. Relationship between clinical features and gastric emptying disturbances in diabetes mellitus. Clin Endocrinol (Oxf). 2009;70:415–20.CrossRefGoogle Scholar
  13. 13.
    Cassilly DW, Wang YR, Friedenberg FK, et al. Symptoms of gastroparesis: use of the gastroparesis cardinal symptom index in symptomatic patients referred for gastric emptying scintigraphy. Digestion. 2008;78:144–51.PubMedCrossRefGoogle Scholar
  14. 14.
    Kong MF, Horowitz M, Jones KL, et al. Natural history of diabetic gastroparesis. Diabetes Care. 1999;22:503–7.PubMedCrossRefGoogle Scholar
  15. 15.
    Jones KL, Russo A, Berry MK, et al. A longitudinal study of gastric emptying and upper gastrointestinal symptoms in patients with diabetes mellitus. Am J Med. 2002;113:449–55.PubMedCrossRefGoogle Scholar
  16. 16.
    Horowitz M, Dent J, Fraser R, et al. Role and integration of mechanisms controlling gastric emptying. Dig Dis Sci. 1994;39:7s–13s.PubMedCrossRefGoogle Scholar
  17. 17.
    Jones KL, Horowitz M, Wishart JM, et al. Relationships between gastric emptying, intragastric meal distribution and blood glucose concentrations in diabetes mellitus. J Nucl Med. 1995;36:2220–8.PubMedGoogle Scholar
  18. 18.
    Merio R, Festa A, Bergmann H, et al. Slow gastric emptying in type I diabetes: relation to autonomic and peripheral neuropathy, blood glucose, and glycemic control. Diabetes Care. 1997;20:419–23.PubMedCrossRefGoogle Scholar
  19. 19.
    Annese V, Bassotti G, Caruso N, et al. Gastrointestinal motor dysfunction, symptoms, and neuropathy in noninsulin-dependent (type 2) diabetes mellitus. J Clin Gastroenterol. 1999;29:171–7.PubMedCrossRefGoogle Scholar
  20. 20.
    Horowitz M, Harding PE, Maddox A, et al. Gastric and oesophageal emptying in insulin-dependent diabetes mellitus. J Gastroenterol Hepatol. 1986;1:97–113.CrossRefGoogle Scholar
  21. 21.
    Rayner CK, Horowitz M. Gastrointestinal motility and glycemic control in diabetes: the chicken and the egg revisited? J Clin Invest. 2006;116:299–302.PubMedCrossRefGoogle Scholar
  22. 22.
    Lurken MS, Parkman HP, Abell TL, et al. Histological changes in idiopathic and diabetic gastroparesis (abstract). Neurogastroenterol Mot. 2009;21(s1):15–98.Google Scholar
  23. 23.
    Choi KM, Gibbons SJ, Nguyen TV, et al. Heme oxygenase-1 protects interstitial cells of Cajal from oxidative stress and reverses diabetic gastroparesis. Gastroenterology. 2008;135:2055–64. 2064 e1-2.PubMedCrossRefGoogle Scholar
  24. 24.
    Kashyap PC, Choi KM, Dutta N, et al. Carbon monoxide reverses diabetic gastroparesis in NOD mice. Am J Physiol Gastrointest Liver Physiol. 2010;298:G1013–9.PubMedCrossRefGoogle Scholar
  25. 25.
    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;106:373–84.PubMedCrossRefGoogle Scholar
  26. 26.
    Gangula PR, Maner WL, Micci MA, et al. Diabetes induces sex-dependent changes in neuronal nitric oxide synthase dimerization and function in the rat gastric antrum. Am J Physiol Gastrointest Liver Physiol. 2007;292:G725–33.PubMedCrossRefGoogle Scholar
  27. 27.
    Dishy V, Cohen Pour M, Feldman L, et al. The effect of sildenafil on gastric emptying in patients with end-stage renal failure and symptoms of gastroparesis. Clin Pharmacol Ther. 2004;76:281–6.PubMedCrossRefGoogle Scholar
  28. 28.
    Fraser R, Horowitz M, Maddox A, et al. Hyperglycaemia slows gastric emptying in type 1 diabetes mellitus. Diabetologia. 1990;30:675–80.CrossRefGoogle Scholar
  29. 29.
    Russo A, Stevens JE, Chen R, et al. Insulin-induced hypoglycemia accelerates gastric emptying of solids and liquids in long-standing type 1 diabetes. J Clin Endocrinol Metab. 2005;90:4489–95.PubMedCrossRefGoogle Scholar
  30. 30.
    Schvarcz E, Palmer M, Aman J, et al. Physiological hyperglycemia slows gastric emptying in normal subjects and patients with insulin-dependent diabetes mellitus. Gastroenterology. 1997;113:60–6.PubMedCrossRefGoogle Scholar
  31. 31.
    Rayner CK, Verhagen MA, Hebbard GS, et al. Proximal gastric compliance and perception of distension in type 1 diabetes mellitus: effects of hyperglycemia. Am J Gastroenterol. 2000;95:1175–83.PubMedCrossRefGoogle Scholar
  32. 32.
    Samsom M, Akkermans LM, Jebbink RJ, et al. Gastrointestinal motor mechanisms in hyperglycaemia induced delayed gastric emptying in type I diabetes mellitus. Gut. 1997;40:641–6.PubMedGoogle Scholar
  33. 33.
    Fraser R, Horowitz M, Dent J. Hyperglycaemia stimulates pyloric motility in normal subjects. Gut. 1991;32:475–8.PubMedCrossRefGoogle Scholar
  34. 34.
    Hasler WL, Soudah HC, Dulai G, et al. Mediation of hyperglycemia-evoked gastric slow-wave dysrhythmias by endogenous prostaglandins. Gastroenterology. 1995;108:727–36.PubMedCrossRefGoogle Scholar
  35. 35.
    Hebbard GS, Sun WM, Dent J, et al. Hyperglycaemia affects proximal gastric motor and sensory function in normal subjects. Eur J Gastroenterol Hepatol. 1996;8:211–7.PubMedCrossRefGoogle Scholar
  36. 36.
    Jones KL, Horowitz M, Berry M, et al. The blood glucose concentration influences postprandial fullness in insulin dependent diabetes mellitus. Diabetes Care. 1997;20:1141–6.PubMedCrossRefGoogle Scholar
  37. 37.
    Kuo P, Gentilcore D, Nair N, et al. The nitric oxide synthase inhibitor, Ng-nitro-l-arginine-methyl-ester, attenuates the delay in gastric emptying induced by hyperglycaemia in healthy humans. Neurogastroenterol Motil. 2009;21:1175–e103.PubMedCrossRefGoogle Scholar
  38. 38.
    Liu M, Seino S, Kirchgessner AL. Identification and characterization of glucoresponsive neurons in the enteric nervous system. J Neurosci. 1999;19:10305–17.PubMedGoogle Scholar
  39. 39.
    Young RL, Sutherland K, Pezos N, et al. Expression of taste molecules in the upper gastrointestinal tract in humans with and without type 2 diabetes. Gut. 2009;58:337–46.PubMedCrossRefGoogle Scholar
  40. 40.
    Monnier L. Is postprandial glucose a neglected cardiovascular risk factor in type 2 diabetes? Eur J Clin Invest. 2000;30 Suppl 2:3–11.PubMedGoogle Scholar
  41. 41.
    Monnier L, Lapinski H, Colette C. Contributions of fasting and postprandial plasma glucose increments to the overall diurnal hyperglycemia of type 2 diabetic patients: variations with increasing levels of HbA(1c). Diabetes Care. 2003;26:881–5.PubMedCrossRefGoogle Scholar
  42. 42.
    Ceriello A, Hanefeld M, Leiter L, et al. Postprandial glucose regulation and diabetic complications. Arch Intern Med. 2004;164:2090–5.PubMedCrossRefGoogle Scholar
  43. 43.
    Horowitz M, Edelbroek MA, Wishart JM, et al. Relationship between oral glucose tolerance and gastric emptying in normal healthy subjects. Diabetologia. 1993;36:857–62.PubMedCrossRefGoogle Scholar
  44. 44.
    Pilichiewicz AN, Chaikomin R, Brennan IM, et al. Load-dependent effects of duodenal glucose on glycemia, gastrointestinal hormones, antropyloroduodenal motility, and energy intake in healthy men. Am J Physiol Endocrinol Metab. 2007;293:E743–53.PubMedCrossRefGoogle Scholar
  45. 45.
    Rayner CK, Ma J, Pilichiewicz A, et al. Effects of variations in duodenal glucose load on ­glycaemia, insulin and GLP-1 in type 2 diabetes (abstract). Diabetologia. 2009;52 Suppl 1:S106–6.Google Scholar
  46. 46.
    O’Donovan DG, Doran S, Feinle-Bisset C, et al. Effect of variations in small intestinal glucose delivery on plasma glucose, insulin, and incretin hormones in healthy subjects and type 2 diabetes. J Clin Endocrinol Metab. 2004;89:3431–5.PubMedCrossRefGoogle Scholar
  47. 47.
    Schwartz JG, McMahan CA, Green GM, et al. Gastric emptying in Mexican Americans compared to non-Hispanic whites. Dig Dis Sci. 1995;40:624–30.PubMedCrossRefGoogle Scholar
  48. 48.
    Gonlachanvit S, Hsu CW, Boden GH, et al. Effect of altering gastric emptying on postprandial plasma glucose concentrations following a physiologic meal in type-II diabetic patients. Dig Dis Sci. 2003;48:488–97.PubMedCrossRefGoogle Scholar
  49. 49.
    Enck P, Dubois D, Marquis P. Quality of life in patients with upper gastrointestinal symptoms: results from the Domestic/International Gastroenterology Surveillance Study (DIGEST). Scand J Gastroenterol Suppl. 1999;231:48–54.PubMedGoogle Scholar
  50. 50.
    Hoogerwerf WA, Pasricha PJ, Kalloo AN, et al. Pain: the overlooked symptom in gastroparesis. Am J Gastroenterol. 1999;94:1029–33.PubMedCrossRefGoogle Scholar
  51. 51.
    Cherian D, Sachdeva P, Fisher RS, et al. Abdominal pain is a frequent symptom of gastroparesis. Clin Gastroenterol Hepatol. 2010;8:676–81.Google Scholar
  52. 52.
    Christensen CJ, Johnson WD, Abell TL. Patients with cyclic vomiting pattern and diabetic gastropathy have more migraines, abnormal electrogastrograms, and gastric emptying. Scand J Gastroenterol. 2008;43:1076–81.PubMedCrossRefGoogle Scholar
  53. 53.
    Schvarcz E, Palmer M, Ingberg CM, et al. Increased prevalence of upper gastrointestinal symptoms in long-term type 1 diabetes mellitus. Diabetic Med. 1996;13:478–81.PubMedCrossRefGoogle Scholar
  54. 54.
    Quan C, Talley NJ, Cross S, et al. Development and validation of the Diabetes Bowel Symptom Questionnaire. Aliment Pharmacol Ther. 2003;17:1179–87.PubMedCrossRefGoogle Scholar
  55. 55.
    Kumar A, Attaluri A, Hashmi S, et al. Visceral hypersensitivity and impaired accommodation in refractory diabetic gastroparesis. Neurogastroenterol Motil. 2008;20:635–42.PubMedCrossRefGoogle Scholar
  56. 56.
    Ishii M, Nakamura T, Kasai F, et al. Erythromycin derivative improves gastric emptying and insulin requirement in diabetic patients with gastroparesis. Diabetes Care. 1997;20:1134–7.PubMedCrossRefGoogle Scholar
  57. 57.
    Nauck MA, Niedereichholz U, Ettler R, et al. Glucagon-like peptide 1 inhibition of gastric emptying outweighs its insulinotropic effects in healthy humans. Am J Physiol. 1997;273:E981–8.PubMedGoogle Scholar
  58. 58.
    Samsom M, Szarka LA, Camilleri M, et al. Pramlintide, an amylin analog, selectively delays gastric emptying: potential role of vagal inhibition. Am J Physiol Gastrointest Liver Physiol. 2000;278:G946–51.PubMedGoogle Scholar
  59. 59.
    Linnebjerg H, Park S, Kothare PA, et al. Effect of exenatide on gastric emptying and relationship to postprandial glycemia in type 2 diabetes. Regul Pept. 2008;151:123–9.PubMedCrossRefGoogle Scholar
  60. 60.
    Lysy J, Israeli E, Strauss-Liviatan N, et al. Relationships between hypoglycaemia and gastric emptying abnormalities in insulin-treated diabetic patients. Neurogastroenterol Motil. 2006;18:433–40.PubMedCrossRefGoogle Scholar
  61. 61.
    Horowitz M, Jones KL, Rayner CK, et al. “Gastric” hypoglycaemia – an important concept in diabetes management. Neurogastroenterol Motil. 2006;18:405–7.PubMedCrossRefGoogle Scholar
  62. 62.
    Ishii M, Nakamura T, Kasai F, et al. Altered postprandial insulin requirement in IDDM patients with gastroparesis. Diabetes Care. 1994;17:901–3.PubMedCrossRefGoogle Scholar
  63. 63.
    Abell TL, Malinowski S, Minocha A. Nutrition aspects of gastroparesis and therapies for drug-refractory patients. Nutr Clin Pract. 2006;21:23–33.PubMedCrossRefGoogle Scholar
  64. 64.
    Groop LC, Luzi L, DeFronzo RA, et al. Hyperglycaemia and absorption of sulphonylurea drugs. Lancet. 1989;2:129–30.PubMedCrossRefGoogle Scholar
  65. 65.
    Jones KL, Tonkin A, Horowitz M, et al. Rate of gastric emptying is a determinant of postprandial hypotension in non-insulin-dependent diabetes mellitus. Clin Sci (Colch). 1998;94:65–70.Google Scholar
  66. 66.
    Gentilcore D, Jones KL, O’Donovan DG, et al. Postprandial hypotension – novel insights into pathophysiology and therapeutic implications. Curr Vasc Pharmacol. 2006;4:161–71.PubMedCrossRefGoogle Scholar
  67. 67.
    Luciano GL, Brennan MJ, Rothberg MB. Postprandial hypotension. Am J Med. 2010;123:281 e1-6.PubMedCrossRefGoogle Scholar
  68. 68.
    Revicki DA, Rentz AM, Dubois D, et al. Development and validation of a patient-assessed gastroparesis symptom severity measure: the Gastroparesis Cardinal Symptom Index. Aliment Pharmacol Ther. 2003;18:141–50.PubMedCrossRefGoogle Scholar
  69. 69.
    Khoo J, Rayner CK, Jones KL, et al. Pathophysiology and management of gastroparesis. Expert Rev Gastroenterol Hepatol. 2009;3:167–81.PubMedCrossRefGoogle Scholar
  70. 70.
    Lee JS, Camilleri M, Zinsmeister AR, et al. Toward office-based measurement of gastric ­emptying in symptomatic diabetics using [13C]octanoic acid breath test. Am J Gastroenterol. 2000;95:2751–61.PubMedCrossRefGoogle Scholar
  71. 71.
    Anderson Jr JH, Brunelle RL, Koivisto VA, et al. Reduction of postprandial hyperglycemia and frequency of hypoglycemia in IDDM patients on insulin-analog treatment. Multicenter Insulin Lispro Study Group. Diabetes. 1997;46:265–70.PubMedCrossRefGoogle Scholar
  72. 72.
    Gentilcore D, Chaikomin R, Jones KL, Russo A, Feinle-Bisset C, Wishart JM, Rayner CK, Horowitz M. Effects of fat on gastric emptying of and the glycemic, insulin, and incretin responses to a carbohydrate meal in type 2 diabetes. J Clin Endocrinol Metab. 2006;91:2062–7.Google Scholar
  73. 73.
    Ma J, Stevens JE, Cukier K, et al. Effects of a protein preload on gastric emptying, glycemia, and gut hormones after a carbohydrate meal in diet-controlled type 2 diabetes. Diabetes Care. 2009;32:1600–2.PubMedCrossRefGoogle Scholar
  74. 74.
    Olausson EA, Alpsten M, Larsson A, et al. Small particle size of a solid meal increases gastric emptying and late postprandial glycaemic response in diabetic subjects with gastroparesis. Diabetes Res Clin Pract. 2008;80:231–7.PubMedCrossRefGoogle Scholar
  75. 75.
    Horowitz M, O’Donovan D, Jones KL, et al. Gastric emptying in diabetes: clinical significance and treatment. Diabet Med. 2002;19:177–94.PubMedCrossRefGoogle Scholar
  76. 76.
    Jones KL, Berry M, Kong M-F, et al. Hyperglycemia attenuates the gastrokinetic effect of erythromycin and affects the perception of postprandial hunger in normal subjects. Diabetes Care. 1999;22:339–44.PubMedCrossRefGoogle Scholar
  77. 77.
    Petrakis IE, Vrachassotakis N, Sciacca V, et al. Hyperglycaemia attenuates erythromycin-induced acceleration of solid-phase gastric emptying in idiopathic and diabetic gastroparesis. Scand J Gastroenterol. 1999;34:396–403.PubMedCrossRefGoogle Scholar
  78. 78.
    Horowitz M, Jones KL, Harding PE, et al. Relationship between the effects of cisapride on gastric emptying and plasma glucose concentrations in diabetic gastroparesis. Digestion. 2002;65:41–6.PubMedCrossRefGoogle Scholar
  79. 79.
    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;53:2072–8.PubMedCrossRefGoogle Scholar
  80. 80.
    Hathaway DK, Abell T, Cardoso S, et al. Improvement in autonomic and gastric function following pancreas-kidney versus kidney-alone transplantation and the correlation with quality of life. Transplantation. 1994;57:816–22.PubMedCrossRefGoogle Scholar
  81. 81.
    Hasler WL. Gastroparesis: symptoms, evaluation, and treatment. Gastroenterol Clin North Am. 2007;36:619–47. ix.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2012

Authors and Affiliations

  • Christopher K. Rayner
    • 1
    • 2
    • 3
    Email author
  • Karen L. Jones
    • 4
  • Michael Horowitz
    • 4
  1. 1.Discipline of MedicineRoyal Adelaide Hospital, University of AdelaideAdelaideAustralia
  2. 2.Department of Gastroenterology and HepatologyRoyal Adelaide HospitalAdelaideAustralia
  3. 3.Centre of Clinical Research Excellence in Nutrition Physiology, Interventions, and OutcomesUniversity of AdelaideAdelaideAustralia
  4. 4.Discipline of MedicineUniversity of Adelaide, Royal Adelaide HospitalAdelaideAustralia

Personalised recommendations