Revisão Revisado por pares

13C-Urea Breath Test for the Diagnosis of Helicobacter pylori Infection in Children: A Systematic Review and Meta-Analysis

2011; Wiley; Volume: 16; Issue: 4 Linguagem: Inglês

10.1111/j.1523-5378.2011.00863.x

ISSN

1523-5378

Autores

Yelda A. Leal, Laura Flores, Ezequiel M. Fuentes‐Pananá, Roberto Cedillo‐Rivera, Javier Torres,

Tópico(s)

Microbial Metabolites in Food Biotechnology

Resumo

HelicobacterVolume 16, Issue 4 p. 327-337 13C-Urea Breath Test for the Diagnosis of Helicobacter pylori Infection in Children: A Systematic Review and Meta-Analysis Yelda A. Leal, Yelda A. Leal Unidad de Investigación Médica Yucatán (UIMY), Unidad Médica de Alta Especialidad de Mérida, Instituto Mexicano del Seguro Social, Mérida, Yuc, MéxicoSearch for more papers by this authorLaura L. Flores, Laura L. Flores Division of Pulmonary and Critical Care Medicine, San Francisco General Hospital and the University of California, San Francisco, CA, USASearch for more papers by this authorEzequiel M. Fuentes-Pananá, Ezequiel M. Fuentes-Pananá Unidad de Investigación Médica en Enfermedades Infecciosas y Parasitarias (UIMEIP), Hospital de Pediatría Centro Médico Nacional Siglo XXI, Instituto Mexicano del Seguro Social, Mexico, DF, MexicoSearch for more papers by this authorRoberto Cedillo-Rivera, Roberto Cedillo-Rivera Unidad de Investigación Médica Yucatán (UIMY), Unidad Médica de Alta Especialidad de Mérida, Instituto Mexicano del Seguro Social, Mérida, Yuc, MéxicoSearch for more papers by this authorJavier Torres, Javier Torres Unidad de Investigación Médica en Enfermedades Infecciosas y Parasitarias (UIMEIP), Hospital de Pediatría Centro Médico Nacional Siglo XXI, Instituto Mexicano del Seguro Social, Mexico, DF, MexicoSearch for more papers by this author Yelda A. Leal, Yelda A. Leal Unidad de Investigación Médica Yucatán (UIMY), Unidad Médica de Alta Especialidad de Mérida, Instituto Mexicano del Seguro Social, Mérida, Yuc, MéxicoSearch for more papers by this authorLaura L. Flores, Laura L. Flores Division of Pulmonary and Critical Care Medicine, San Francisco General Hospital and the University of California, San Francisco, CA, USASearch for more papers by this authorEzequiel M. Fuentes-Pananá, Ezequiel M. Fuentes-Pananá Unidad de Investigación Médica en Enfermedades Infecciosas y Parasitarias (UIMEIP), Hospital de Pediatría Centro Médico Nacional Siglo XXI, Instituto Mexicano del Seguro Social, Mexico, DF, MexicoSearch for more papers by this authorRoberto Cedillo-Rivera, Roberto Cedillo-Rivera Unidad de Investigación Médica Yucatán (UIMY), Unidad Médica de Alta Especialidad de Mérida, Instituto Mexicano del Seguro Social, Mérida, Yuc, MéxicoSearch for more papers by this authorJavier Torres, Javier Torres Unidad de Investigación Médica en Enfermedades Infecciosas y Parasitarias (UIMEIP), Hospital de Pediatría Centro Médico Nacional Siglo XXI, Instituto Mexicano del Seguro Social, Mexico, DF, MexicoSearch for more papers by this author First published: 18 July 2011 https://doi.org/10.1111/j.1523-5378.2011.00863.xCitations: 70 Reprint requests to: Yelda A. Leal, Unidad de Investigación Médica Yucatán, Unidad Médica de Alta Especialidad del Centro Médico Nacional “Ignacio García Téllez” Mérida Yucatán, Instituto Mexicano del Seguro Social, Calle 34 #439 x 41 Colonia Industrial (Ex-terrenos del Fénix, Hospital T1), Mérida, Yucatán 97150, México. E-mail: [email protected] Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat Abstract Background: The 13C-urea breath test (13C-UBT) is a safe, noninvasive and reliable method for diagnosing H. pylori infection in adults. However, the test has shown variable accuracy in the pediatric population, especially in young children. We aimed to carry out a systematic review and meta-analysis to evaluate the performance of the 13C-UBT diagnostic test for H. pylori infection in children. Methods: We conducted a systematic review of the PubMed, Embase and Liliacs databases including studies from January 1998 to May 2009. Selection criteria included studies with at least 30 children and reporting the comparison of 13C-UBT against a gold standard for H. pylori diagnosis. Thirty-one articles and 135 studies were included for analysis. Children were stratified in subgroups of 6 years (sensitivity 96.6%, specificity 97.7%, LR+ 42.6, LR− 0.04, DOR 1042.7), 3, greater variability in accuracy estimates and on average a few percentage points lower, particularly specificity, in children ≤6 years (sensitivity 95%, specificity 93.5%, LR+ 11.7, LR− 0.12, DOR 224.8). Therefore, the meta-analysis shows that the 13C-UBT test is less accurate for the diagnosis of H. pylori infection in young children, but adjusting cutoff value, pretest meal, and urea dose, this accuracy can be improved. References 1 Perez-Perez GI, Rothenbacher D, Brenner H. Epidemiology of Helicobacter pylori infection. Helicobacter 2004; 9(Suppl 1): 1–6. 2 Suerbaum S, Michetti P. Helicobacter pylori infection. N Engl J Med 2002; 347: 1175–86. 3 Kusters J, van Vliet A, Kuipers E. Pathogenesis of Helicobacter pylori infection. Clin Microbiol Rev 2006; 19: 449–90. 4 Drumm B, Day A, Gold B, et al. European Society for Paediatric Gastroenterology, Hepatology and Nutrition. Helicobacter pylori and peptic ulcer: Working Group Report of the second World Congress of Pediatric Gastroenterology, Hepatology, and Nutrition. J Pediatr Gastroenterol Nutr 2004; 39(Suppl 2): S626–31. 5 Czinn S, Gold B, Dickinson C, et al. Research agenda for pediatric gastroenterology, hepatology and nutrition: acid-peptic diseases. Report of the North American Society for Pediatric Gastroenterology, Hepatology and Nutrition for the Children’s Digestive Health and Nutrition Foundation. J Pediatr Gastroenterol Nutr 2002; 35(Suppl 3): S250–3. 6 Koletzko S. Noninvasive diagnostic tests for Helicobacter pylori infection in children. Can J Gastroenterol 2005; 19: 433–9. 7 Mobley H, Island M, Hausinger R. Molecular biology of microbial ureases. Microbiol Rev 1995; 59: 451–80. 8 Stingl K, Altendorf K, Bakker E. Acid survival of Helicobacter pylori: how does urease activity trigger cytoplasmic pH homeostasis? Trends Microbiol 2002; 10: 70–4. 9 Yoshiyama H, Nakazawa T. Unique mechanism of Helicobacter pylori for colonizing the gastric mucus. Microbes Infect 2000; 2: 55–60. 10 Graham D, Klein P, Evans D Jr, et al. Campylobacter pylori detected noninvasively by the 13C-urea breath test. Lancet 1987; 1: 1174–7. 11 Marshall B, Francis G, Langton S, et al. Rapid urease test in the management of Campylobacter pyloridis associated gastritis. Am J Gastroenterol 1987; 3: 200–10. 12 Marshall B, Surveyor I. Carbon-14 urea breath test for the diagnosis of Campylobacter pylori associated gastritis. J Nucl Med 1988; 29: 11–6. 13 Monteiro L, Oleastro M, Lehours P, Megraud F. Diagnosis of Helicobacter pylori infection. Helicobacter 2009; 14: 8–14. 14 Kawakami E, Machado R, Reber M, Patricio F. 13 C-urea breath test with infrared spectroscopy for diagnosing Helicobacter pylori infection in children and adolescents. J Pediatr Gastroenterol Nutr 2002; 35: 39–43. 15 Parente F, Bianchi P. The (13)C-urea breath test for non-invasive diagnosis of Helicobacter pylori infection: which procedure and which measuring equipment? Eur J Gastroenterol Hepatol 2001; 13: 803–6. 16 Slater C, Preston T, Weaver L. Is there an advantage in normalising the results of the Helicobacter pylori [13C] urea breath test for CO2 production rate in children? Isotopes Environ Health Stud 2004; 40: 89–98. 17 Gisbert J, Pajares J. Review article: 13C-urea breath test in the diagnosis of Helicobacter pylori infection – a critical review. Aliment Pharmacol Ther 2004; 20: 1001–17. 18 Bourke B, Ceponis P, Chiba N, et al. Canadian Helicobacter Study Group Consensus Conference: update on the approach to Helicobacter pylori infection in children and adolescents – an evidence-based evaluation. Can J Gastroenterol 2005; 19: 399–408. 19 Roberts A, Childs S, Rubin G, de Wit N. Tests for Helicobacter pylori infection: a critical appraisal from primary care. Fam Pract 2000; 17: S12–20. 20 De Carvalho Costa Cardinali L, Rocha G, Rocha A, et al. Evaluation of [13C] urea breath test and Helicobacter pylori stool antigen test for diagnosis of H. pylori infection in children from a developing country. J Clin Microbiol 2003; 41: 3334–5. 21 Imrie C, Rowland M, Bourke B, Drumm B. Limitations to carbon 13-labeled urea breath testing for Helicobacter pylori in infants. J Pediatr 2001; 139: 734–7. 22 Kato S, Nakayama K, Minoura T, et al. Comparison between the 13C-urea breath test and stool antigen test for the diagnosis of childhood Helicobacter pylori infection. J Gastroenterol 2004; 39: 1045–50. 23 Deville WL, Buntinx F, Bouter LM, et al. Conducting systematic reviews of diagnostic studies: didactic guidelines. BMC Med Res Methodol 2002; 2: 9–21. 24 Lijmer J, Bossuyt P, Heisterkamp S. Exploring sources of heterogeneity in systematic reviews of diagnostic tests. Stat Med 2002; 21: 1525–37. 25 Pai M, McCulloch M, Gorman J, et al. Systematic reviews and meta-analyses: an illustrated, step-by-step guide. Natl Med J India 2004; 17: 86–95. 26 Deeks J, Altman D. Diagnostic tests 4: likelihood ratios. BMJ 2004; 329: 168–9. 27 Glas AS, Lijmer JG, Prins MH, et al. The diagnostic odds ratio: a single indicator of test performance. J Clin Epidemiol 2003; 56: 1129–35. 28 Smidt N, Rutjes A, van der Windt D, et al. Reproducibility of the STARD checklist: an instrument to assess the quality of reporting of diagnostic accuracy studies. BMC Med Res Methodol 2006; 6: 12–21. 29 Zamora J, Abraira V, Muriel A, Khan K, Coomarasamy A. Meta-DiSc: a software for meta-analysis of test accuracy data. BMC Med Res Methodol 2006; 6: 31–42. 30 Walter S. Properties of the summary receiver operating characteristic (SROC) curve for diagnostic test data. Stat Med 2002; 21: 1237–56. 31 Hino B, Eliakim R, Levine A, et al. Comparison of invasive and non-invasive tests diagnosis and monitoring of Helicobacter pylori infection in children. J Pediatr Gastroenterol Nutr 2004; 39: 519–23. 32 Bazzoli F, Cecchini L, Corvaglia L, et al. Validation of the 13C-urea breath test for the diagnosis of Helicobacter pylori infection in children: a multicenter study. Am J Gastroenterol 2000; 95: 646–50. 33 Rowland M, Lambert I, Gormally S, et al. Carbon 13-labeled urea breath test for the diagnosis of Helicobacter pylori infection in children. J Pediatr 1997; 131: 815–20. 34 Kato S, Ozawa K, Konno M, et al. Diagnostic accuracy of the 13C-urea breath test for childhood Helicobacter pylori infection: a multicenter Japanese study. Am J Gastroenterol 2002; 97: 1668–73. 35 Machado RS, Patricio FR, Kawakami E. 13C-urea breath test to diagnose Helicobacter pylori infection in children aged up to 6 years. Helicobacter 2004; 9: 39–45. 36 Frenck R Jr, Fathy H, Sherif M, et al. Sensitivity and specificity of various tests for the diagnosis of Helicobacter pylori in Egyptian children. Pediatrics 2006; 118: e1195–202. 37 Rutigliano V, Ierardi E, Francavilla R, et al. Helicobacter pylori and nonulcer dyspepsia in childhood: clinical pattern, diagnostic techniques, and bacterial strains. J Pediatr Gastroenterol Nutr 1999; 28: 296–300. 38 Ni Y, Lin J, Huang S, Yang J, Chang M. Accurate diagnosis of Helicobacter pylori infection by stool antigen test and 6 other currently available tests in children. J Pediatr 2000; 136: 823–7. 39 Vincent P, Michaud L, Martin de L, Benon B, Turck D, Gottrand F. 13C-urea breath test and gastric mucosal colonization by Helicobacter pylori in children: quantitative relation and usefulness for diagnosis of infection. Helicobacter 1999; 4: 233–7. 40 Konstantopoulos N, Russmann H, Tasch C, et al. Evaluation of the Helicobacter pylori stool antigen test (HpSA) for detection of Helicobacter pylori infection in children. Am J Gastroenterol 2001; 96: 677–83. 41 Eltumi M, Brueton M, Francis N. Diagnosis of Helicobacter pylori gastritis in children using the 13C urea breath test. J Clin Gastroenterol 1999; 28: 238–40. 42 Parejo C, Olivares M, Escobar C, Jimenez A, de Rafael N, Camarero S. [A comparative analysis of diagnostic methods for Helicobacter pylori infection in children]. An Esp Pediatr 1998; 49: 257–63. 43 Gonzalez-Cuevas A, Juncosa T, Jene M, et al. [Helicobacter pylori infections: antigen detection in stool samples]. Enferm Infecc Microbiol Clin 2001; 19: 49–52. 44 Megraud F. Comparison of non-invasive tests to detect Helicobacter pylori infection in children and adolescents: results of a multicenter European study. J Pediatr 2005; 146: 198–203. 45 Dondi E, Rapa A, Boldorini R, Fonio P, Zanetta S, Oderda G. High accuracy of noninvasive tests to diagnose Helicobacter pylori infection in very young children. J Pediatr 2006; 149: 817–21. 46 Canete A, Abunaji Y, varez-Calatayud G, et al. Breath test using a single 50-mg dose of 13C-urea to detect Helicobacter pylori infection in children. J Pediatr Gastroenterol Nutr 2003; 36: 105–11. 47 Cadranel S, Corvaglia L, Bontems P, et al. Detection of Helicobacter pylori infection in children with a standardized and simplified 13C-urea breath test. J Pediatr Gastroenterol Nutr 1998; 27: 275–80. 48 Kalach N, Briet F, Raymond J, et al. The 13carbon urea breath test for the noninvasive detection of Helicobacter pylori in children: comparison with culture and determination of minimum analysis requirements. J Pediatr Gastroenterol Nutr 1998; 26: 291–6. 49 Yanez P, la Garza A, Perez G, Cabrera L, Munoz O, Torres J. Comparison of invasive and noninvasive methods for the diagnosis and evaluation of eradication of Helicobacter pylori infection in children. Arch Med Res 2000; 31: 415–21. 50 Corvaglia L, Bontems P, Devaster J, et al. Accuracy of serology and 13C-urea breath test for detection of Helicobacter pylori in children. Pediatr Infect Dis J 1999; 18: 976–9. 51 Kindermann A, Demmelmair H, Koletzko B, Krauss-Etschmann S, Wiebecke B, Koletzko S. Influence of age on 13C-urea breath test results in children. J Pediatr Gastroenterol Nutr 2000; 30: 85–91. 52 Yang H, Seo J. Diagnostic accuracy of the C-urea breath test in children: adjustment of the cut-off value according to age. J Gastroenterol Hepatol 2005; 20: 264–9. 53 Yang H, Ko J, Seo J. Does the diagnostic accuracy of the 13C-urea breath test vary with age even after the application of urea hydrolysis rate? Helicobacter 2008; 13: 239–44. 54 Elitsur Y, Tolia V, Gilger M, et al. Urea breath test in children: the United States prospective, multicenter study. Helicobacter 2009; 14: 134–40. 55 Delvin E, Brazier J, Deslandres C, Alvarez F, Russo P, Seidman E. Accuracy of the [13C]-urea breath test in diagnosing Helicobacter pylori gastritis in pediatric patients. J Pediatr Gastroenterol Nutr 1999; 28: 59–62. 56 Levine A, Shevah O, Miloh T, et al. Validation of a novel real time 13C urea breath test for rapid evaluation of Helicobacter pylori in children and adolescents. J Pediatr 2004; 145: 112–4. 57 Herold R, Becker M. 13C-urea breath test threshold calculation and evaluation for the detection of Helicobacter pylori infection in children. BMC Gastroenterol 2002; 2: 12–7. 58 Aas J, Paster B, Stokes L, Olsen I, Dewhirst F. Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 2005; 43: 5721–32. 59 Bik E, Eckburg P, Gill S, et al. Molecular analysis of the bacterial microbiota in the human stomach. Proc Natl Acad Sci USA 2006; 103: 732–7. 60 Peng N, Lai K, Liu R, et al. Clinical significance of oral urease in diagnosis of Helicobacter pylori infection by [13C] urea breath test. Dig Dis Sci 2001; 46: 1772–8. 61 Vaira D, Gatta L, Ricci C, Di M, Lanzini A. Accuracy of urea breath tests tablets after 10 minutes compared with standard 30 minutes to diagnose and monitoring Helicobacter pylori infection: a randomized controlled trial. J Clin Gastroenterol 2009; 43: 693–4. 62 Klein P, Malaty H, Czinn S, Emmons S, Martin R, Graham D. Normalizing results of 13C-urea breath testing for CO2 production rates in children. J Pediatr Gastroenterol Nutr 1999; 29: 297–301. 63 Rektorschek M, Weeks D, Sachs G, Melchers K. Influence of pH on metabolism and urease activity of Helicobacter pylori. Gastroenterology 1998; 115: 628–41. 64 Graham D, Opekun A, Jogi M, et al. False negative urea breath tests with H2-receptor antagonists: interactions between Helicobacter pylori density and pH. Helicobacter 2004; 9: 17–27. 65 Epple H, Kirstein F, Bojarski C, et al. 13C-urea breath test in Helicobacter pylori diagnosis and eradication. Correlation to histology, origin of ‘false’ results, and influence of food intake. Scand J Gastroenterol 1997; 32: 308–14. 66 Vakil N. Review article: the cost of diagnosing Helicobacter pylori infection. Aliment Pharmacol Ther 2001; 15: 10–5. 67 Perri F, Pastore M, Clemente R, et al. Helicobacter pylori infection may undergo spontaneous eradication in children: a 2-year follow-up study. J Pediatr Gastroenterol Nutr 1998; 27: 181–3. 68 Phillips CV, Goodman KJ. Interpreting data in the face of competing explanations: assessing the hypothesis that observed spontaneous clearance of Helicobacter pylori was all measurement error. Int J Epidemiol 2009; 38: 1110–7. 69 Leal-Herrera Y, Torres J, Monath T, et al. High rates of recurrence and of transient reinfections of Helicobacter pylori in a population with high prevalence of infection. Am J Gastroenterol 2003; 98: 2395–402. 70 Goodman KJ, O’Rourke K, Day S, et al. Dynamics of Helicobacter pylori infection in a US-Mexico cohort during the first two years of life. Int J Epidemiol 2005; 34: 1348–55. 71 Nurgalieva Z, Opekun A, Graham D. Problem of distinguishing false-positive tests from acute or transient Helicobacter pylori infections. Helicobacter 2006; 11: 69–74. 72 Leal YA, Cedillo-Rivera R, Simon JA, Velázquez JR, Flores LL, Torres J. Utility of stool sample-based tests for the diagnosis of Helicobacter pylori infection in children. J Pediatr Gastroenterol Nutr 2011; 52: 718–28. 73 Rutjes A, Reitsma J, Di N, Smidt N, van Rijn J, Bossuyt P. Evidence of bias and variation in diagnostic accuracy studies. CMAJ 2006; 174: 469–76. Citing Literature Volume16, Issue4August 2011Pages 327-337 ReferencesRelatedInformation

Referência(s)
Altmetric
PlumX