Is Gastroparesis Found More Frequently in Patients with Cystic Fibrosis? A Systematic Review

Juan E Corral, Corey W Dye, Maria R Mascarenhas, Jamie S Barkin, Matthias Salathe, Baharak Moshiree, Juan E Corral, Corey W Dye, Maria R Mascarenhas, Jamie S Barkin, Matthias Salathe, Baharak Moshiree

Abstract

Cystic fibrosis (CF) is associated with different gastrointestinal motility disturbances and syndromes. We aim to assess gastric emptying in patients with CF compared to healthy controls by a systematic review of existing literature. Medical databases and abstracts from major gastroenterology and CF meetings were reviewed. Emptying times in CF patients were compared with healthy controls using random effects models. Subgroup analysis stratified results by age and diagnostic modality. Nineteen studies from 7 countries included 574 subjects (359 CF patients and 215 controls). Using pooled analysis frequency of gastroparesis was high (38%, 95% CI 30-45%) but results were highly dependent on the diagnostic modality. Delayed gastric emptying is more common in CF compared to general population. Scintigraphy identified rapid gastric emptying in a subgroup of CF patients, but this finding disappeared with adequate pancreatic enzyme replacement and after other diagnostic modalities were included.

Figures

Figure 1
Figure 1
Selection of studies for inclusion in systematic review. DDW: Digestive Disease Week, ACG: American College of Gastroenterology, EUG: United European Gastroenterology, NACFC: North American Cystic Fibrosis Conference, and ECFS: European Cystic Fibrosis Society.
Figure 2
Figure 2
Forest plot graph for frequency of gastroparesis in cystic fibrosis, divided by measuring technique.

References

    1. Eggermont E. Gastrointestinal manifestations in cystic fibrosis. European Journal of Gastroenterology and Hepatology. 1996;8(8):731–738.
    1. Malfroot A., Dab I. New insights on gastro-oesophageal reflux in cystic fibrosis by longitudinal follow up. Archives of Disease in Childhood. 1991;66(11):1339–1345. doi: 10.1136/adc.66.11.1339.
    1. Milla P. J. Cystic fibrosis: present and future. Digestion. 1998;59(5):579–588. doi: 10.1159/000007533.
    1. Rovner A. J., Schall J. I., Mondick J. T., Zhuang H., Mascarenhas M. R. Delayed small bowel transit in children with cystic fibrosis and pancreatic insufficiency. Journal of Pediatric Gastroenterology and Nutrition. 2013;57(1):81–84. doi: 10.1097/MPG.0b013e318290d112.
    1. De Boeck K., Delbeke I., Eggermont E., Veereman-Wauters G., Ghoos Y. Lipid digestion in cystic fibrosis: comparison of conventional and high-lipase enzyme therapy using the mixed-triglyceride breath test. Journal of Pediatric Gastroenterology and Nutrition. 1998;26(4):408–411. doi: 10.1097/00005176-199804000-00009.
    1. Nousia-Arvanitakis S. Cystic fibrosis and the pancreas: recent scientific advances. Journal of Clinical Gastroenterology. 1999;29(2):138–142. doi: 10.1097/00004836-199909000-00007.
    1. Bronstein M. N., Sokol R. J., Abman S. H., et al. Pancreatic insufficiency, growth, and nutrition in infants identified by newborn screening as having cystic fibrosis. The Journal of Pediatrics. 1992;120(4, part 1):533–540. doi: 10.1016/s0022-3476(05)82478-3.
    1. Bruno M. J., Haverkort E. B., Tytgat G. N. J., Van Leeuwen D. J. Maldigestion associated with exocrine pancreatic insufficiency: implications of gastrointestinal physiology and properties of enzyme preparations for a cause-related and patient-tailored treatment. The American Journal of Gastroenterology. 1995;90(9):1383–1393.
    1. Symonds E. L., Omari T. I., Webster J. M., Davidson G. P., Butler R. N. Relation between pancreatic lipase activity and gastric emptying rate in children with cystic fibrosis. The Journal of Pediatrics. 2003;143(6):772–775. doi: 10.1067/s0022-3476(03)00581-x.
    1. Keshavarzian A., Isaac R. M. Erythromycin accelerates gastric emptying of indigestible solids and transpyloric migration of the tip of an enteral feeding tube in fasting and fed states. The American Journal of Gastroenterology. 1993;88(2):193–197.
    1. Larson J. M., Tavakkoli A., Drane W. E., Toskes P. P., Moshiree B. Advantages of azithromycin over erythromycin in improving the gastric emptying half-time in adult patients with gastroparesis. Journal of Neurogastroenterology and Motility. 2010;16(4):407–413. doi: 10.5056/jnm.2010.16.4.407.
    1. Kuo B., Maneerattanaporn M., Lee A. A., et al. Generalized transit delay on wireless motility capsule testing in patients with clinical suspicion of gastroparesis, small intestinal dysmotility, or slow transit constipation. Digestive Diseases and Sciences. 2011;56(10):2928–2938. doi: 10.1007/s10620-011-1751-6.
    1. Stroup D. F., Berlin J. A., Morton S. C., et al. Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis of Observational Studies in Epidemiology (MOOSE) group. The Journal of the American Medical Association. 2000;283(15):2008–2012. doi: 10.1001/jama.283.15.2008.
    1. Hedsund C., Gregersen T., Joensson I. M., Olesen H. V., Krogh K. Gastrointestinal transit times and motility in patients with cystic fibrosis. Scandinavian Journal of Gastroenterology. 2012;47(8-9):920–926. doi: 10.3109/00365521.2012.699548.
    1. Gelfond D., Ma C., Semler J., Borowitz D. Intestinal pH and gastrointestinal transit profiles in cystic fibrosis patients measured by wireless motility capsule. Digestive Diseases and Sciences. 2013;58(8):2275–2281. doi: 10.1007/s10620-012-2209-1.
    1. Neumann D., Pozler O., Vorisek V., et al. The gastric emptying of a solid meal in cystic fibrosis patients assessed by the 13C-octanoic acid breath test. Cesko-Slovenska Pediatrie. 2003;58(6):374–377.
    1. Hauser B., De Schepper J., Malfroot A., et al. Gastric emptying and gastro-oesophageal reflux in children with cystic fibrosis. Journal of Cystic Fibrosis. 2016 doi: 10.1016/j.jcf.2015.12.015.
    1. Pauwels A., Blondeau K., Mertens V., et al. Gastric emptying and different types of reflux in adult patients with cystic fibrosis. Alimentary Pharmacology and Therapeutics. 2011;34(7):799–807. doi: 10.1111/j.1365-2036.2011.04786.x.
    1. Hauser B., Malfroot A., De Schutter I., et al. 240 Is gastric emptying delayed in children with cystic fibrosis? Journal of Cystic Fibrosis. 2013;12, article S109 doi: 10.1016/s1569-1993(13)60381-1.
    1. Davidson A. G., Nadel H., Wong L. T., editors. Delayed gastric empyting in cystic fibrosis. Proceedings of the North American Cystic Fibrosis Conference (NACFC '95); 1995.
    1. Carney B. I., Jones K. L., Horowitz M., Wei Ming Sun, Penagini R., Meyer J. H. Gastric emptying of oil and aqueous meal components in pancreatic insufficiency: effects of posture and on appetite. American Journal of Physiology—Gastrointestinal and Liver Physiology. 1995;268(6, part 1):G925–G932.
    1. Collins C. E., Francis J. L., Thomas P., Henry R. L., O'Loughlin E. V. Gastric emptying time is faster in cystic fibrosis. Journal of Pediatric Gastroenterology and Nutrition. 1997;25(5):492–498. doi: 10.1097/00005176-199711000-00002.
    1. Munck A., Bonnin F., Gerardin M., et al., editors. Oral erythromycin effect on gastric emptying in cystic fibrosis patients. Proceedings of the North American Cystic Fibrosis Conference (NACFC '97); 1997.
    1. Couturier O., Bodet-Milin C., Querellou S., Carlier T., Turzo A., Bizais Y. Gastric scintigraphy with a liquid-solid radiolabelled meal: performances of solid and liquid parameters. Nuclear Medicine Communications. 2004;25(11):1143–1150. doi: 10.1097/00006231-200411000-00013.
    1. King S. J., Button B. M., Kelly M. J., et al., editors. Delayed gastric emptying is common in adults with cystic fibrosis and is associated with lower body mass index. Proceedings of the North American Cystic Fibrosis Conference (NACFC '06); November 2006; Denver, Colo, USA.
    1. Tonelli A. R., Drane W. E., Collins D. P., Nichols W., Antony V. B., Olson E. L. Erythromycin improves gastric emptying half-time in adult cystic fibrosis patients with gastroparesis. Journal of Cystic Fibrosis. 2009;8(3):193–197. doi: 10.1016/j.jcf.2009.02.001.
    1. Luu K., Chilvers M., Nadel H. Cisapride and its effect on gastric emtpying in pediatric cystic fibrosis patients. Proceedings of the North American Cystic Fibrosis Conference (NACFC '11); 2011; Anaheim, Calif, USA.
    1. Kuo P., Stevens J. E., Russo A., et al. Gastric emptying, incretin hormone secretion, and postprandial glycemia in cystic fibrosis—effects of pancreatic enzyme supplementation. Journal of Clinical Endocrinology and Metabolism. 2011;96(5):E851–E855. doi: 10.1210/jc.2010-2460.
    1. Mendez B. M., Davis C. S., Weber C., Joehl R. J., Fisichella P. M. Gastroesophageal reflux disease in lung transplant patients with cystic fibrosis. The American Journal of Surgery. 2012;204(5):e21–e26. doi: 10.1016/j.amjsurg.2012.07.019.
    1. Wells G., Shea B., O'Connell D., et al. The Newcastle-Ottawa Scale (NOS) for Assessing the Quality of Nonrandomised Studies in Meta-Analyses. Ottawa, Canada: Ottawa Hospital Research Institute; 2014. .
    1. Abell T. L., Camilleri M., Donohoe K., et al. Consensus recommendations for gastric emptying scintigraphy: a joint report of the American neurogastroenterology and motility society and the society of nuclear medicine. The American Journal of Gastroenterology. 2008;103(3):753–763. doi: 10.1111/j.1572-0241.2007.01636.x.
    1. Parkman H. P., Hasler W. L., Fisher R. S. American Gastroenterological Association medical position statement: diagnosis and treatment of gastroparesis. Gastroenterology. 2004;127(5):1589–1591. doi: 10.1053/j.gastro.2004.09.054.
    1. Jung H.-K., Choung R. S., Locke G. R., III, et al. The incidence, prevalence, and outcomes of patients with gastroparesis in Olmsted County, Minnesota, from 1996 to 2006. Gastroenterology. 2009;136(4):1225–1233. doi: 10.1053/j.gastro.2008.12.047.
    1. Frank L., Kleinman L., Ganoczy D., et al. Upper gastrointestinal symptoms in North America: prevalence and relationship to healthcare utilization and quality of life. Digestive Diseases and Sciences. 2000;45(4):809–818. doi: 10.1023/a:1005468332122.
    1. Jones K. L., Russo A., Stevens J. E., Wishart J. M., Berry M. K., Horowitz M. Predictors of delayed gastric emptying in diabetes. Diabetes Care. 2001;24(7):1264–1269. doi: 10.2337/diacare.24.7.1264.
    1. Kong M.-F., Horowitz M., Jones K. L., Wishart J. M., Harding P. E. Natural history of diabetic gastroparesis. Diabetes Care. 1999;22(3):503–507. doi: 10.2337/diacare.22.3.503.
    1. Horowitz M., Maddox A. F., Wishart J. M., Harding P. E., Chatterton B. E., Shearman D. J. C. Relationships between oesophageal transit and solid and liquid gastric emptying in diabetes mellitus. European Journal of Nuclear Medicine. 1991;18(4):229–234. doi: 10.1007/BF00186645.
    1. Parkman H. P., Yates K., Hasler W. L., et al. Clinical features of idiopathic gastroparesis vary with sex, body mass, symptom onset, delay in gastric emptying, and gastroparesis severity. Gastroenterology. 2011;140(1):101–115. doi: 10.1053/j.gastro.2010.10.015.
    1. Borowitz D., Gelfond D. Intestinal complications of cystic fibrosis. Current Opinion in Pulmonary Medicine. 2013;19(6):676–680. doi: 10.1097/MCP.0b013e3283659ef2.
    1. De Lisle R. C., Meldi L., Mueller R. Intestinal smooth muscle dysfunction develops postnatally in cystic fibrosis mice. Journal of Pediatric Gastroenterology and Nutrition. 2012;55(6):689–694. doi: 10.1097/MPG.0b013e3182638bf4.
    1. van der Sijp J. R. M., Kamm M. A., Nightingale J. M. D., et al. Disturbed gastric and small bowel transit in severe idiopathic constipation. Digestive Diseases and Sciences. 1993;38(5):837–844. doi: 10.1007/bf01295909.
    1. Hasler W. L. Gastroparesis: pathogenesis, diagnosis and management. Nature Reviews Gastroenterology and Hepatology. 2011;8(8):438–453. doi: 10.1038/nrgastro.2011.116.
    1. Moran A., Brunzell C., Cohen R. C., et al. Clinical care guidelines for cystic fibrosis-related diabetes: a position statement of the American Diabetes Association and a clinical practice guideline of the Cystic Fibrosis Foundation, endorsed by the Pediatric Endocrine Society. Diabetes Care. 2010;33(12):2697–2708. doi: 10.2337/dc10-1768.
    1. Saliakellis E., Fotoulaki M. Gastroparesis in children. Annals of Gastroenterology. 2013;26(3):204–211.
    1. Smout A., Horowitz M., Armstrong D. Methods to study gastric emptying. Frontiers in gastric emptying. Digestive Diseases and Sciences. 1994;39(12, supplement):130S–132S.
    1. Hunt J. N., Stubbs D. F. The volume and energy content of meals as determinants of gastric emptying. The Journal of Physiology. 1975;245(1):209–225. doi: 10.1113/jphysiol.1975.sp010841.
    1. Govin B., Nazareth D., Mohan K., et al., editors. Assessment of gastric emptying in cystic fibrosis using a novel bedside ultrasonographic technique. Proceedings of the North American Cystic Fibrosis Conference (NACFC '12); 2012.
    1. Bodet-Milin C., Querellou S., Oudoux A., et al. Delayed gastric emptying scintigraphy in cystic fibrosis patients before and after lung transplantation. Journal of Heart and Lung Transplantation. 2006;25(9):1077–1083. doi: 10.1016/j.healun.2006.04.013.
    1. Dellon E. S., Morgan D. R., Mohanty S. P., Davis K., Aris R. M. High incidence of gastric bezoars in cystic fibrosis patients after lung transplantation. Transplantation. 2006;81(8):1141–1146. doi: 10.1097/01.tp.0000205813.54136.85.
    1. Chogle A., Saps M. Gastroparesis in children: the benefit of conducting 4-hour scintigraphic gastric-emptying studies. Journal of Pediatric Gastroenterology and Nutrition. 2013;56(4):439–442. doi: 10.1097/mpg.0b013e31827a789c.
    1. Ludbrook J. Detecting systematic bias between two raters. Clinical and Experimental Pharmacology and Physiology. 2004;31(1-2):113–115. doi: 10.1111/j.1440-1681.2004.03960.x.

Source: PubMed

Sponsorzy i współpracownicy

Warunki medyczne

Interwencje lekowe

3
Subskrybuj