Download PDF
Exp Clin Endocrinol Diabetes 2003; 111(4): 223-229
DOI: 10.1055/s-2003-40467
Article

J. A. Barth Verlag in Georg Thieme Verlag Stuttgart · New York

Gastric Emptying of Solid and Liquid Meals in Healthy Controls Compared with Long-Term Type-1 Diabetes Mellitus under Optimal Glucose Control

C. Folwaczny 1 , R. Wawarta 2 , B. Otto 1 , S. Friedrich 3 , R. Landgraf 4 , R. L. Riepl 5
  • 1City Department of Gastroenterology, Ludwig-Maximilians-University, Munich, Germany
  • 2Department of Gastroenterology, Augsburg Hospital, Augsburg, Germany
  • 3Department of Gastroenterology, Weiden Hospital, Weiden, Germany
  • 4City Department of Endocrinology, Ludwig-Maximilians-University, Munich, Germany
  • 5Department of Gastroenterology, Erding Hospital, Erding, Germany
Further Information

Publication History

Received: May 8, 2002 First decision: October 20, 2002

Accepted: January 10, 2003

Publication Date:
07 July 2003 (online)

Also available at
    Permissions and Reprints

Abstract

Background

Neuropathy of the enteric nervous system and hyperglycaemia are regarded as the main causes of diabetic gastroparesis.

Patients and Methods

In ten patients with Type-1 diabetes mellitus and sensomotoric neuropathy gastric emptying half times were compared with ten healthy controls by employing the 13C-octanoic acid and the 13C-sodiumacetate breath test, resp., following the intake of equally composed and isocaloric liquid and solid meals. Plasma glucose concentrations were controlled by permanent intravenous administration of insulin.

Results

In diabetes mellitus gastric emptying half times after the intake of the liquid meal (p < 0.05) but not after ingestion of the solid meal were slightly prolonged. Gastric emptying half times in patients and controls were not different when liquid and solid meals were compared.

Conclusions

Acute hyperglycaemia appears to be more important than the neuropathy of the enteric nervous system in the pathophysiology of diabetic gastroparesis. The rate of gastric emptying is obviously not dependent on the phase of a meal, but rather on the composition and the caloric content.

Key words

Gastric emptying - diabetes mellitus - solid - liquid - glucose control

References

  • 1 Annese V, Bassotti G, Caruso N, De Cosmo S, Gabbrielli A, Modoni S, Frusciante V, Andriulli A. Gastrointestinal motor dysfunction, symptoms, and neuropathy in noninsulin-dependent (type 2) diabetes mellitus.  J Clin Gastroenterol. 1999;  29 171-177
    CrossrefPubMedGoogle Scholar
  • 2 Asakawa A, Inui A, Momose K, Ueno N, Fujino M A, Kasuga M. Motilin increases food intake in mice.  Peptides. 1997;  19 987-990
    PubMedGoogle Scholar
  • 3 Bargen J A, Bollmann J L, Kepler E J. The “diarrhea of diabetes” and steatorrhea of pancreatic insufficiency.  Proc Mayo Clin. 1936;  11 737-742
    PubMedGoogle Scholar
  • 4 Barnett J L, Owyang C. Serum glucose concentration as a modulator of interdigestive gastric motility.  Gastroenterology. 1988;  94 739-744
    CrossrefPubMedGoogle Scholar
  • 5 Benini L, Castellani G, Brighenti F, Heaton K W, Brentegani M T, Casiraghi M C, Sembenini C, Pellegrini N, Fioretta A, Minniti G. et al . Gastric emptying of a solid meal is accelerated by the removal of dietary fibre naturally present in food.  Gut. 1995;  36 825-830
    PubMedGoogle Scholar
  • 6 Braden B, Adams S, Duan L P, Orth K H, Maul F D, Lembcke B, Hor G, Caspary W F. The 13C acetate breath test accurately reflects gastric emptying of liquids in both liquid and semisolid test meals.  Gastroenterology. 1995;  108 1048-155
    PubMedGoogle Scholar
  • 7 Brophy C M, Moore J G, Christian P E, Egger M J, Taylor A T. Variability of gastric emptying measurements in man employing standardized radiolabeled meals.  Dig Dis Sci. 1986;  31 799-806
    CrossrefPubMedGoogle Scholar
  • 8 Chey W D, Kim M, Hasler W L, Owyang C. Hyperglycemia alters perception of rectal distention and blunts the rectoanal inhibitory reflex in healthy volunteers.  Gastroenterology. 1995;  108 1700-1708
    PubMedGoogle Scholar
  • 9 Christian P E, Moore J G, Sorenson J A, Coleman R E, Weich D M. Effects of meal size and correction technique on gastric emptying time: studies with two tracers and opposed detectors.  J Nucl Med. 1980;  21 883-885
    PubMedGoogle Scholar
  • 10 Cortot A, Philips S F, Malagelada J R. Parallel gastric emptying of nonhydrolyzable fat and water after a solid-liquid meal in humans.  Gastroenterology. 1982;  82 877-881
    PubMedGoogle Scholar
  • 11 Dyrberg T, Benn J, Christiansen J S, Hilsted J, Nerup J. Prevalence of diabetic autonomic neuropathy measured by simple bedside tests.  Diabetologia. 1981;  20 190-194
    PubMedGoogle Scholar
  • 12 Eliasson B, Bjornsson E, Urbanavicius V, Andersson H, Fowelin J, Attvall S, Abrahamsson H, Smith U. Hyperinsulinaemia impairs gastrointestinal motility and slows carbohydrate absorption.  Diabetologia. 1995;  38 79-85
    CrossrefPubMedGoogle Scholar
  • 13 Feighner S D, Tan C P, McKee K K, Palyha O C, Hreniuk D L, Pong S S, Austin C P, Figueroa D, MacNeil D, Cascieri M A, Nargund R, Bakshi R, Abramovitz M, Stocco R, Kargman S, O'Neill G, Van Der Ploeg L H, Evans J, Patchett A A, Smith R G, Howard A D. Receptor for motilin identified in the human gastrointestinal system.  Science. 1999;  284 2184-2188
    CrossrefPubMedGoogle Scholar
  • 14 Folwaczny C, Hundegger K, Volger C, Sorodoc J, Kuhn M, Tatsch K, Landgraf R, Karbach U. Measurement of transit disorders in different gastrointestinal segments of patients with diabetes mellitus in relation to duration and severity of the disease by use of the metal-detector test.  Z Gastroenterol. 1995;  33 517-526
    PubMedGoogle Scholar
  • 15 Folwaczny C, Riepl R, Tschop M, Landgraf R. Gastrointestinal involvement in diabetes mellitus: Part I (first of two parts), epidemiology, pathophysiology, clinical findings.  Z Gastroenterol. 1999;  37 803-815
    PubMedGoogle Scholar
  • 16 Folwaczny C, Chang J K, Tschöp M. Ghrelin and motilin: Two sides of the same coin?.  Eur J Endocrinol. 2001;  144 R1-3
    CrossrefPubMedGoogle Scholar
  • 17 Fraser R, Fuller J, Horowitz M, Dent J. Effect of insulin-induced hypoglycaemia on antral, pyloric and duodenal motility in fasting subjects.  Clin Sci. 1991 a;  81 281-285
    PubMedGoogle Scholar
  • 18 Fraser R, Horowitz M, Dent J. Hyperglycaemia stimulates pyloric motility in normal subjects.  Gut. 1991 b;  32 475-478
    CrossrefPubMedGoogle Scholar
  • 19 Fraser R J, Horowitz M, Maddox A F, Harding P E, Chatterton B E, Dent J. Hyperglycaemia slows gastric emptying in type 1 (insulin-dependent) diabetes mellitus.  Diabetologia. 1990;  33 675-680
    CrossrefPubMedGoogle Scholar
  • 20 Garthwaite T L. Peripheral motilin administration stimulates feeding in fasted rats.  Peptides. 1985;  6 41-44
    PubMedGoogle Scholar
  • 21 Ghoos Y F, Maes B D, Geypens B J, Mys G, Hiele M I, Rutgeerts P J, Vantrappen G. Measurement of gastric emptying rate of solids by means of a carbon-labeled octanoic acid breath test.  Gastroenterology. 1993;  104 1640-1647
    CrossrefPubMedGoogle Scholar
  • 22 Glasbrenner B, Pieramico O, Brecht-Krauss D, Baur M, Malfertheiner P. Gastric emptying of solids and liquids in obesity.  Clin Investig. 1993;  71 542-546
    PubMedGoogle Scholar
  • 23 Hasler W L, Kim M S, Chey W D, Stevenson V, Stein B, Owyang C. Central cholinergic and alpha-adrenergic mediation of gastric slow wave dysrhythmias evoked during motion sickness.  Am J Physiol. 1995 a;  268 G539-547
    PubMedGoogle Scholar
  • 24 Hasler W L, Kurosawa S, Takahashi T, Feng H, Gaginella T S, Owyang C. Bradykinin acting on B2 receptors contracts colon circular muscle cells by IP3 generation and adenylate cyclase inhibition.  J Pharmacol Exp Ther. 1995 b;  273 344-350
    PubMedGoogle Scholar
  • 25 Hasler W L, Soudah H C, Dulai G, Owyang C. Mediation of hyperglycemia-evoked gastric slow-wave dysrhythmias by endogenous prostaglandins.  Gastroenterology. 1995 c;  108 727-736
    PubMedGoogle Scholar
  • 26 Heading R C, Tothill P, McLoughlin G P, Shearman D J. Gastric emptying rate measurement in man. A double isotope scanning technique for simultaneous study of liquid and solid components of a meal.  Gastroenterology. 1976;  71 45-50
    PubMedGoogle Scholar
  • 27 Hebbard G S, Reid K, Sun W M, Horowitz M, Dent J. Postural changes in proximal gastric volume and pressure measured using a gastric barostat.  Neurogastroenterol Motil. 1995;  7 169-174
    PubMedGoogle Scholar
  • 28 Hebbard G S, Sun W M, Dent J, Horowitz M. Hyperglycaemia affects proximal gastric motor and sensory function in normal subjects.  Eur J Gastroenterol Hepatol. 1996;  8 211-217
    CrossrefPubMedGoogle Scholar
  • 29 Holzäpfel A, Festa A, Stacher-Janotta G, Bergmann H, Shnawa N, Brannath W, Schernthaner G, Stacher G. Gastric emptying in Type II (non-insulin-dependent) diabetes mellitus before and after therapy readjustment: no influence of actual blood glucose concentration.  Diabetologia. 1999;  42 1410-1412
    CrossrefPubMedGoogle Scholar
  • 30 Horowitz M, Collins J P, Shearman D J. Effect of increasing the caloric/osmotic content of the liquid component of a mixed solid and liquid meal on gastric emptying in obese subjects.  Hum Nutr Clin Nutr. 1986;  40 51-56
    PubMedGoogle Scholar
  • 31 Horowitz M, Harding P E, Maddox A F, Wishart J M, Akkermans L M, Chatterton B E, Shearman D J. Gastric and oesophageal emptying in patients with type 2 (non-insulin-dependent) diabetes mellitus.  Diabetologia. 1989 a;  32 151-159
    CrossrefPubMedGoogle Scholar
  • 32 Horowitz M, Maddox A, Bochner M, Wishart J, Bratasiuk R, Collins P, Shearman D. Relationships between gastric emptying of solid and caloric liquid meals and alcohol consumption.  Am J Physiol. 1989 b;  257 G291-298
    PubMedGoogle Scholar
  • 33 Horowitz M, Edelbroek M, Fraser R, Maddox A, Wishart J. Disordered gastric motor function in diabetes mellitus. Recent insights into prevalence, pathophysiology, clinical relevance, and treatment.  Scand J Gastroenterol. 1991 a;  26 673-684
    PubMedGoogle Scholar
  • 34 Horowitz M, Maddox A F, Wishart J M, Harding P E, Chatterton B E, Shearman D J. Relationships between oesophageal transit and solid and liquid gastric emptying in diabetes mellitus.  Eur J Nucl Med. 1991 b;  18 229-234
    PubMedGoogle Scholar
  • 35 Horowitz M, Wishart J M, Jones K L, Hebbard G S. Gastric emptying in diabetes: An overview.  Diabet Med. 1996;  13 S16-22
    PubMedGoogle Scholar
  • 36 Howard A D, Feighner S D, Cully D F, Arena J P, Liberator P A, Rosenblum C I, Hamelin M, Hreniuk D L, Palyha O C, Anderson J, Paress P S, Diaz C, Chou M, Liu K K, McKee K K, Pong S S, Chaung L Y, Elbrecht A, Dashkevicz M, Heavens R, Rigby M, Sirinathsinghji D J, Dean D C, Melillo D G, Van der Ploeg L H. A receptor in pituitary and hypothalamus that functions in growth hormone release.  Science. 1996;  273 974-977
    CrossrefPubMedGoogle Scholar
  • 37 Jian R, Ruskone A, Filali A, Ducrot F, Rain J D, Bernier J J. Effect of the increase of the caloric load of a meal on gastric emptying of its solid and liquid phases.  Gastroenterol Clin Biol. 1986;  10 821-826
    PubMedGoogle Scholar
  • 38 Jebbink R J, Samsom M, Bruijs P P, Bravenboer B, Akkermans L M, Vanberge-Henegouwen G P, Smout A J. Hyperglycemia induces abnormalities of gastric myoelectrical activity in patients with type I diabetes mellitus.  Gastroenterology. 1994;  107 1390-1397
    PubMedGoogle Scholar
  • 39 Jeyarajah R, Samarawickrama P, Jameel M M. Autonomic function tests in non-insulin dependent diabetic patients and apparently healthy volunteers.  J Chronic Dis. 1986;  39 479-484
    CrossrefPubMedGoogle Scholar
  • 40 Kawagishi T, Nishizawa Y, Okuno Y, Shimada H, Inaba M, Konishi T, Morii H. Antroduodenal motility and transpyloric fluid movements in patients with diabetes studied with duplex sonography.  Gastroenterology. 1994;  107 403-409
    PubMedGoogle Scholar
  • 41 Keshavarzian A, Dunne M, Iber F L. Gallbladder volume and emptying in insulin-requiring male diabetics.  Dig Dis Sci. 1987;  32 824-828
    CrossrefPubMedGoogle Scholar
  • 42 Kris M G, Yeh S D, Gralla R J, Young C W. Simultaneous estimation of liquid and solid gastric emptying using radiolabelled egg and water in supine normal subjects.  Int J Rad Appl Instrum B. 1986;  13 629-631
    PubMedGoogle Scholar
  • 43 Lartigue S, Bizais Y, Des Varannes S B, Murat A, Pouliquen B, Galmiche J P. Inter- and intrasubject variability of solid and liquid gastric emptying parameters. A scintigraphic study in healthy subjects and diabetic patients.  Dig Dis Sci. 1994;  39 109-115
    PubMedGoogle Scholar
  • 44 Lundgren O. The stomach talks with the pituitary.  Gut. 2000;  47 168-169
    CrossrefPubMedGoogle Scholar
  • 45 Lyrenas E B, Olsson E H, Arvidsson U C, Orn T J, Spjuth J H. Prevalence and determinants of solid and liquid gastric emptying in unstable type I diabetes. Relationship to postprandial blood glucose concentrations.  Diabetes Care. 1997;  20 413-438
    PubMedGoogle Scholar
  • 46 MacGregor I, Parent J, Meyer J H. Gastric emptying of liquid meals and pancreatic and biliary secretion after subtotal gastrectomy or truncal vagotomy and pyloroplasty in man.  Gastroenterology. 1977;  72 195-205
    PubMedGoogle Scholar
  • 47 Malagelada J R, Robertson J S, Brown M L, Remington M, Duenes J A, Thomforde G M, Carryer P W. Intestinal transit of solid and liquid components of a meal in health.  Gastroenterology. 1984;  87 1255-1263
    PubMedGoogle Scholar
  • 48 Maxton D G, Whorwell P J. Functional bowel symptoms in diabetes: the role of autonomic neuropathy.  Postgrad Med J. 1991;  67 991-993
    PubMedGoogle Scholar
  • 49 Moore J G, Christian P E, Coleman R E. Gastric emptying of varying meal weight and composition in man. Evaluation of dual liquid- and solid-phase isotopic method.  Dig Dis Sci. 1981;  26 16-22
    CrossrefPubMedGoogle Scholar
  • 50 Moore J G, Christian P E, Brown J A, Brophy C, Datz F, Taylor A, Alazraki N. Influence of meal weight and caloric content on gastric emptying of meals in man.  Dig Dis Sci. 1984;  29 513-519
    CrossrefPubMedGoogle Scholar
  • 51 Notivol R, Carrio I, Cano L, Estorch M, Vilardell F. Gastric emptying of solid and liquid meals in healthy young subjects.  Scand J Gastroenterol. 1984;  19 1107-1113
    PubMedGoogle Scholar
  • 52 Oster-Jorgensen E, Pedersen S A, Larsen M L. The influence of induced hyperglycemia on gastric emptying in healthy humans.  Scand J Lab Clin Invest. 1990;  50 831-836
    PubMedGoogle Scholar
  • 53 Petrakis I E, Chalkiadakis G, Vrachassotakis N, Sciacca V, Vassilakis S J, Xynos E. Induced hyperglycemia attenuates erythromycin-induced acceleration of hypertonic liquid-phase gastric emptying in Type-1 Diabetes.  Dig Dis. 1999;  17 241-247
    CrossrefPubMedGoogle Scholar
  • 54 Reilly Jr J A, Forst C F, Quigley E M, Rikkers L F. Gastric emptying of liquids and solids in the portal hypertensive rat.  Dig Dis Sci. 1990;  35 781-786
    CrossrefPubMedGoogle Scholar
  • 55 Rundles R W. Diabetic neuropathy: General review with report of 125 cases.  Medicine. 1945;  24 111-160
    CrossrefPubMedGoogle Scholar
  • 56 Schvarcz E, Palmer M, Aman J, Berne C. Hypoglycemia increases the gastric emptying rate in healthy subjects.  Diabet Care. 1995;  18 674-676
    PubMedGoogle Scholar
  • 57 Schvarcz E, Palmer M, Aman J, Horowitz M, Stridsberg M, Berne C. Physiological hyperglycemia slows gastric emptying in normal subjects and patients with insulin-dependent diabetes mellitus.  Gastroenterology. 1997;  113 60-66
    CrossrefPubMedGoogle Scholar
  • 58 Sims M A, Hasler W L, Chey W D, Kim M S, Owyang C. Hyperglycaemia inhibits mechanoreceptor-mediated gastrocolonic responses and colonic peristaltic reflexes in healthy humans.  Gastroenterology. 1995;  108 350-359
    CrossrefPubMedGoogle Scholar
  • 59 Toepfer M, Folwaczny C, Lochmuller H, Schroeder M, Riepl R L, Pongratz D, Muller-Felber W. Noninvasive 13C-octanoic acid breath test shows delayed gastric emptying in patients with amyotrophic lateral sclerosis.  Digestion. 1999;  60 567-571
    CrossrefPubMedGoogle Scholar
  • 60 Tomasetto C, Karam S M, Ribieras S, Masson R, Lefebvre O, Staub A, Alexander G, Chenard M P, Rio M C. Identification and characterization of a novel gastric peptide hormone: The motilin-related peptide.  Gastroenterology. 2000;  119 395-405
    PubMedGoogle Scholar
  • 61 Tschöp M, Wawarta R, Riepl R L, Landgraf R, Folwaczny C. Postprandial decrease of circulating human ghrelin levels.  J Endocrinol Invest. 2001;  24 RC19-RC21
    PubMedGoogle Scholar
  • 62 Urbain J L, Siegel J A, Mortelmans L, van Cutsem E, van den Maegdenbergh V, de Roo M. Effect of solid-meal caloric content on gastric emptying kinetics of solids and liquids.  Nuklearmedizin. 1989;  28 120-123
    PubMedGoogle Scholar
  • 63 Wegener M, Borsch G, Schaffstein J, Luerweg C, Leverkus F. Gastrointestinal transit disorders in patients with insulin-treated diabetes mellitus.  Dig Dis. 1990;  8 23-36
    PubMedGoogle Scholar

PD Dr. med. Christian Folwaczny

Chirurgische Klinik und Medizinische Poliklinik-Innenstadt
Ludwig-Maximilians-Universität München

Nussbaumstraße 20

80336 München

Germany

Phone: + 498951602625

Fax: + 49 89 51 60 41 87

Email: Christian.Folwaczny@medinn.med.uni-muenchen.de

      >