Helicobacter pylori infection in children: an overview of diagnostic methods

  • Parisa Sabbagh
  • Mostafa Javanian
  • Veerendra Koppolu
  • VeneelaKrishna Rekha Vasigala
  • Soheil EbrahimpourEmail author


Children differ from adults regarding Helicobacter pylori (H. pylori) infection in many terms. H. pylori infection represents a key factor in the pathogenesis of duodenal ulcer and chronic gastritis in children. H. pylori infection causes some extraintestinal diseases as well as gastrointestinal diseases. Although, among these illnesses in children, symptoms like recurrent abdominal pain are not specific. Moreover, the role of the pathogen in the growth faltering, iron deficiency anemia, and asthma still remains controversial. A reliable method to detect H. pylori infection is a crucial issue, sand is still a matter of active debate. The tests applied for H. pylori diagnosis are grouped as either invasive or non-invasive methods. Invasive methods consist of endoscopic evaluation, the rapid urease test (RUT), histology, and bacterial culture. Non-invasive tests include the urea breath test (UBT), stool antigen test (SAT), serology, and molecular diagnostic approaches. Use of endoscopy is a pre-requisite for all invasive methods and poses difficulties in children as it is a difficult procedure and requires patient’s cooperation. For this reason, the non-invasive tests have been commonly used in children, although their accuracy is not very reliable in some cases. Invasive tests may be opted to confirm the diagnosis as and when needed. This review presents the diagnostic tests used to detect H. pylori infection in children.


Helicobacter pylori Diagnosis Children 



The authors express their appreciation to Vice Chancellor for Research and Technology of Babol University of Medical Sciences for supporting this research and Marzieh Nourollahzadeh for her advice as a translator of this article.

Specific author contributions

P.S and S.E conceived the study; M.J, V.K, V.K.R.V, and S.E collected all data; P.S and S.E drafted the manuscript; and all authors commented on the drafts of the manuscript and approved the final draft of the paper.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study received the approval from the Babol University of Medical Science, Ethical Committee.

Informed consent

There is no informed consent for this review article.


  1. 1.
    Warren JR, Marshall B (1983) Unidentified curved bacilli on gastric epithelium in active chronic gastritis. Lancet 321(8336):1273–1275Google Scholar
  2. 2.
    Marshall B, Warren JR (1984) Unidentified curved bacilli in the stomach of patients with gastritis and peptic ulceration. Lancet 323(8390):1311–1315Google Scholar
  3. 3.
    Ebrahimpour S, Esmaeili H, Ghadimi R (2017) Food bioactive componts, a possible adjuvant for H. pylori eradication. Caspian J Intern Med 8(2):131Google Scholar
  4. 4.
    Suerbaum S, Michetti P (2002) Helicobacter pylori infection. N Engl J Med 347(15):1175–1186Google Scholar
  5. 5.
    Ohata H, Kitauchi S, Yoshimura N, Mugitani K, Iwane M, Nakamura H, Yoshikawa A, Yanaoka K, Arii K, Tamai H (2004) Progression of chronic atrophic gastritis associated with Helicobacter pylori infection increases risk of gastric cancer. Int J Cancer 109(1):138–143Google Scholar
  6. 6.
    Hill R, Pearman J, Worthy P, Caruso V, Goodwin S, Blincow E (1986) Campylobacter pyloridis and gastritis in children. Lancet 327(8477):387Google Scholar
  7. 7.
    Sabbagh P, Mohammadnia-Afrouzi M, Javanian M, Babazadeh A, Koppolu V, Vasigala VR, Nouri HR, Ebrahimpour S (2018) Diagnostic methods for Helicobacter pylori infection: ideals, options, and limitations. J Clin Microbiol Infect Dis 38(1):55–66Google Scholar
  8. 8.
    Nejati S, Karkhah A, Darvish H, Validi M, Ebarhimpour S, Nouri HR (2018) Influence of Helicobacter pylori virulence factors CagA and VacA on pathogenesis of gastrointestinal disorders. Microb Pathog​​117:43–48Google Scholar
  9. 9.
    Tokudome S, Hosono A, Suzuki S, Ghadimi R, Tanaka T, Ichikawa H, Miyata M, Marumoto M, Agawa H, Arakawa K, Ando R, Hattori N, Shibata K, Yang Z (2006) Helicobacter pylori infection as an essential factor for stomach cancer. Asian Pac J Cancer Prev 7(1):163Google Scholar
  10. 10.
    Ernst PB, Gold BD (1999) Helicobacter pylori in childhood: new insights into the immunopathogenesis of gastric disease and implications for managing infection in children. J Pediatr Gastroenterol Nutr 28(5):462–473Google Scholar
  11. 11.
    Kusters JG, van Vliet AH, Kuipers EJ (2006) Pathogenesis of Helicobacter pylori infection. Clin Microbiol Rev 19(3):449–490Google Scholar
  12. 12.
    Correa P, Piazuelo MB (2008) Natural history of Helicobacter pylori infection. Dig Liver Dis 40(7):490–496Google Scholar
  13. 13.
    Imrie C, Rowland M, Bourke B, Drumm B (2001) Is Helicobacter pylori infection in childhood a risk factor for gastric cancer? Pediatrics 107(2):373–380Google Scholar
  14. 14.
    Sicinschi LA, Correa P, Bravo LE, Peek RM Jr, Wilson KT, Loh JT, Yepez MC, Gold BD, Thompson DT, Cover TL (2012) Non-invasive genotyping of Helicobacter pylori cagA, vacA, and hopQ from asymptomatic children. Helicobacter 17(2):96–106Google Scholar
  15. 15.
    Czinn SJ (2005) Helicobacter pylori infection: detection, investigation, and management. J Pediatr 146(3):S21–S26Google Scholar
  16. 16.
    Ou Z, Xiong L, Li D-Y, Geng L, Li L, Chen P, Yang M, Zeng Y, Zhou Z, Xia H (2013) Evaluation of a new fluorescence quantitative PCR test for diagnosing Helicobacter pylori infection in children. BMC Gastroenterol 13(1):7Google Scholar
  17. 17.
    Koletzko S, Jones NL, Goodman KJ, Gold B, Rowland M, Cadranel S, Chong S, Colletti RB, Casswall T, Elitsur Y (2011) Evidence-based guidelines from ESPGHAN and NASPGHAN for Helicobacter pylori infection in children. J Pediatr Gastroenterol Nutr 53(2):230–243Google Scholar
  18. 18.
    Karkhah A, Ebrahimpour S, Rostamtabar M, Koppolu V, Darvish S, Vasigala VKR, Validi M, Nouri HR (2018) Helicobacter pylori evasion strategies of the host innate and adaptive immune responses to survive and develop gastrointestinal disease. Microbiol Res​​ 218:49–57Google Scholar
  19. 19.
    Austin J, Doig P, Stewart M (1992) Structural comparison of urease and a GroEL analog from Helicobacter pylori. J Bacteriol 174(22):7470–7473Google Scholar
  20. 20.
    Amieva MR, El-Omar EM (2008) Host-bacterial interactions in Helicobacter pylori infection. Gastroenterology 134(1):306–323Google Scholar
  21. 21.
    Leunk R, Johnson P, David B, Kraft W, Morgan D (1988) Cytotoxic activity in broth-culture filtrates of Campylobacter pylori. J Med Microbiol 26(2):93–99Google Scholar
  22. 22.
    Willhite DC, Blanke SR (2004) Helicobacter pylori vacuolating cytotoxin enters cells, localizes to the mitochondria, and induces mitochondrial membrane permeability changes correlated to toxin channel activity. Cell Microbiol 6(2):143–154Google Scholar
  23. 23.
    Yamasaki E, Wada A, Kumatori A, Nakagawa I, Funao J, Nakayama M, Hisatsune J, Kimura M, Moss J, Hirayama T (2006) Helicobacter pylori vacuolating cytotoxin induces activation of the proapoptotic protein Bax and Bak, leading to cytochrome c release and cell death, independent of. J Biol Chem​ 281(16):11250–11259Google Scholar
  24. 24.
    Noto JM, Peek RM (2012) Helicobacter pylori: an overview. Helicobacter species. Springer, pp 7–10Google Scholar
  25. 25.
    Cadamuro ACT, Rossi AFT, Maniezzo NM, Silva AE (2014) Helicobacter pylori infection: host immune response, implications on gene expression and microRNAs. World J Gastroenterol: WJG 20(6):1424Google Scholar
  26. 26.
    Larussa T, Leone I, Suraci E, Imeneo M, Luzza F (2015) Helicobacter pylori and T helper cells: mechanisms of immune escape and tolerance. J Immunol Res 2015:981328–981328Google Scholar
  27. 27.
    Rajindrajith S, Devanarayana NM, De Silva HJ (2009) Helicobacter pylori infection in children. Saudi J Gastroenterol 15(2):86Google Scholar
  28. 28.
    Bellack N, Koehoorn M, MacNab Y, Morshed M (2006) A conceptual model of water’s role as a reservoir in Helicobacter pylori transmission: a review of the evidence. Epidemiol Infect 134(3):439–449Google Scholar
  29. 29.
    Dube C, Nkosi T, Clarke A, Mkwetshana N, Green E, Ndip R (2009) Helicobacter pylori antigenemia in an asymptomatic population of Eastern Cape Province, South Africa: public health implications. Rev Environ Health 24(3):249–255Google Scholar
  30. 30.
    Konno M, S-i Y, Suga T, Takahashi M, Sato K, Fujii N (2008) Predominance of mother-to-child transmission of Helicobacter pylori infection detected by random amplified polymorphic DNA fingerprinting analysis in Japanese families. Pediatr Infect Dis J 27(11):999–1003Google Scholar
  31. 31.
    Weyermann M, Rothenbacher D, Brenner H (2009) Acquisition of Helicobacter pylori infection in early childhood: independent contributions of infected mothers, fathers, and siblings. Am J Gastroenterol 104(1):182Google Scholar
  32. 32.
    Zabala Torrres B, Lucero Y, Lagomarcino AJ, Orellana-Manzano A, George S, Torres JP, O'ryan M (2017) Prevalence and dynamics of Helicobacter pylori infection during childhood. Helicobacter 22(5):e12399Google Scholar
  33. 33.
    Opekun AR, Gilger MA, Denyes SM, Nirken MH, Philip SP, Osato MS, Malaty HM, Hicks J, Graham DY (2000) Helicobacter pylori infection in children of Texas. J Pediatr Gastroenterol Nutr 31(4):405–410Google Scholar
  34. 34.
    Wizla-Derambure N, Michaud L, Ategbo S, Vincent P, Ganga-Zandzou S, Turck D, Gottrand F (2001) Familial and community environmental risk factors for Helicobacter pylori infection in children and adolescents. J Pediatr Gastroenterol Nutr 33(1):58–63Google Scholar
  35. 35.
    Mourad-Baars PE, Verspaget HW, Mertens BJ, Mearin ML (2007) Low prevalence of Helicobacter pylori infection in young children in the Netherlands. Eur J Gastroenterol Hepatol 19(3):213–216Google Scholar
  36. 36.
    Bureš J, Kopáčová M, Koupil I, Seifert B, Fendrichová MŠ, Špirková J, Voříšek V, Rejchrt S, Douda T, Král N (2012) Significant decrease in prevalence of Helicobacter pylori in the Czech Republic. World J Gastroenterol: WJG 18(32):4412Google Scholar
  37. 37.
    Jafri W, Yakoob J, Abid S, Siddiqui S, Awan S, Nizami S (2010) Helicobacter pylori infection in children: population-based age-specific prevalence and risk factors in a developing country. Acta Paediatr 99(2):279–282Google Scholar
  38. 38.
    Poddar U, Yachha SK (2007) Helicobacter pylori in children: an Indian perspective​​Indian Pediatr 44(10):761–770Google Scholar
  39. 39.
    Naous A, Al-Tannir M, Naja Z, Ziade F, El-Rajab M (2007) Fecoprevalence and determinants of Helicobacter pylori infection among asymptomatic children in Lebanon. J Med Liban 55(3):138–144Google Scholar
  40. 40.
    Mohammad MA, Hussein L, Coward A, Jackson SJ (2008) Prevalence of Helicobacter pylori infection among Egyptian children: impact of social background and effect on growth. Public Health Nutr 11(3):230–236Google Scholar
  41. 41.
    Sýkora J, Siala K, Varvařovská J, Pazdiora P, Pomahačová R, Huml M (2009) Epidemiology of Helicobacter pylori infection in asymptomatic children: a prospective population-based study from the Czech Republic. Application of a monoclonal-based antigen-in-stool enzyme immunoassay. Helicobacter 14(4):286–297Google Scholar
  42. 42.
    Staat MA, Kruszon-Moran D, McQuillan GM, Kaslow RA (1996) A population-based serologic survey of Helicobacter pylori infection in children and adolescents in the United States. J Infect Dis 174(5):1120–1123Google Scholar
  43. 43.
    Patterson T, Straten E, Jimenez S (2012) The prevalence of Helicobacter pylori antibody in different age groups in Central Texas. Clin Lab Sci 25(2):102Google Scholar
  44. 44.
    Tkachenko MA, Zhannat NZ, Erman LV, Blashenkova EL, Isachenko SV, Isachenko OB, Graham DY, Malaty HM (2007) Dramatic changes in the prevalence of Helicobacter pylori infection during childhood: a 10-year follow-up study in Russia. J Pediatr Gastroenterol Nutr 45(4):428–432Google Scholar
  45. 45.
    Fock KM, Ang TL (2010) Epidemiology of Helicobacter pylori infection and gastric cancer in Asia. J Gastroenterol Hepatol 25(3):479–486Google Scholar
  46. 46.
    De Martel C, Ferlay J, Franceschi S, Vignat J, Bray F, Forman D, Plummer M (2012) Global burden of cancers attributable to infections in 2008: a review and synthetic analysis. Lancet Oncol 13(6):607–615Google Scholar
  47. 47.
    Sachs G, Scott DR (2012) Helicobacter pylori: eradication or preservation. F1000 Med Rep 4:7Google Scholar
  48. 48.
    Frank F, Stricker T, Stallmach T, Braegger CP (2000) Helicobacter pylori infection in recurrent abdominal pain. J Pediatr Gastroenterol Nutr 31(4):424–427Google Scholar
  49. 49.
    Kimia A, Zahavi I, Shapiro R, Rosenbach Y, Hirsh A, Druzd T, Yahav J, Dinari G (2000) The role of Helicobacter pylori and gastritis in children with recurrent abdominal pain. Isr Med Assoc J 2(2):126–128Google Scholar
  50. 50.
    Masoodpoor N, Sheikhvatan M (2010) Helicobacter pylori infection in Iranian children with recurrent abdominal pain. Trop Gastroenterol 29(4):221–223Google Scholar
  51. 51.
    Spee LA, Madderom MB, Pijpers M, van Leeuwen Y, Berger MY (2010) Association between Helicobacter pylori and gastrointestinal symptoms in children. Pediatrics 125(3):e651–e669Google Scholar
  52. 52.
    Moon A, Solomon A, Beneck D, Cunningham-Rundles S (2009) Positive association between Helicobacter pylori and gastroesophageal reflux disease in children. J Pediatr Gastroenterol Nutr 49(3):283Google Scholar
  53. 53.
    Emiroglu HH, Sokucu S, Suoglu OD, Gulluoglu M, Gokce S (2010) Is there a relationship between Helicobacter pylori infection and erosive reflux disease in children? Acta Paediatr 99(1):121–125Google Scholar
  54. 54.
    Daugule I, Rumba I, Alksnis J, Ejderhamn J (2007) Helicobacter pylori infection among children with gastrointestinal symptoms: a high prevalence of infection among patients with reflux oesophagitis. Acta Paediatr 96(7):1047–1049Google Scholar
  55. 55.
    Ierardi E, Giangaspero A, Losurdo G, Giorgio F, Amoruso A, De V (2014) Quadruple rescue erapy after first and second line failure for Helicobacter pylori treatment: comparison between two tetracycline-based regimens. J Gastrointestin Liver Dis 23(4):367–370Google Scholar
  56. 56.
    Wu J, Chan F, Ching J, Leung W, Hui Y, Leong R, Chung S, Sung J (2004) Effect of Helicobacter pylori eradication on treatment of gastro-oesophageal reflux disease: a double blind, placebo controlled, randomised trial. Gut 53(2):174–179Google Scholar
  57. 57.
    Wu J, Chan F, Wong S, Lee Y, Leung W, Sung J (2002) Effect of Helicobacter pylori eradication on oesophageal acid exposure in patients with reflux oesophagitis. Aliment Pharmacol Ther 16(3):545–552Google Scholar
  58. 58.
    Gold BD (2003) Outcomes of pediatric gastroesophageal reflux disease: in the first year of life, in childhood, and in adults... oh, and should we really leave Helicobacter pylori alone? J Pediatr Gastroenterol Nutr 37:S33–S39Google Scholar
  59. 59.
    Masrour-Roudsari J, Ebrahimpour S (2017) Causal role of infectious agents in cancer: an overview. Caspian J Intern Med 8(3):153–158Google Scholar
  60. 60.
    Nourollahpour Shiadeh M, Riahi SM, Adam I, Saber V, Behboodi Moghadam Z, Armon B, Spotin A, Nazari Kangavari H, Rostami A (2019) Helicobacter pylori infection and risk of preeclampsia: a systematic review and meta-analysis. J Matern Fetal Neonatal Med 32(2):324–331Google Scholar
  61. 61.
    Kim SS, Ruiz VE, Carroll JD, Moss SF (2011) Helicobacter pylori in the pathogenesis of gastric cancer and gastric lymphoma. Cancer Lett 305(2):228–238Google Scholar
  62. 62.
    Rowland M, Bourke B, Drumm B (2004) Helicobacter pylori and peptic ulcer disease. Pediatric gastrointestinal disease, 4th edn. BC Decker Co., Canada, pp 491–505Google Scholar
  63. 63.
    Macarthur C, Saunders N, Feldman W (1995) Helicobacter pylori, gastroduodenal disease, and recurrent abdominal pain in children. Jama 273(9):729–734Google Scholar
  64. 64.
    Yeung C-Y, Lee H-C (2017) Paediatric Helicobacter pylori infection in Taiwan: current status and perspectives. Gastroenterology 6(1):90–97Google Scholar
  65. 65.
    Choi J (2003) Does Helicobacter pylori infection relate to iron deficiency anaemia in prepubescent children under 12 years of age? Acta Paediatr 92(8):970–972Google Scholar
  66. 66.
    Choe Y, Kim S, Hong Y (2003) The relationship between Helicobacter pylori infection and iron deficiency: seroprevalence study in 937 pubescent children. Arch Dis Child 88(2):178–178Google Scholar
  67. 67.
    Sherman P, Czinn S, Drumm B, Gottrand F, Kawakami E, Madrazo A, Oderda G, Seo J-K, Sullivan P, Toyoda S (2002) Helicobacter pylori infection in children and adolescents: working group report of the first world congress of pediatric gastroenterology, hepatology, and nutrition. J Pediatr Gastroenterol Nutr 35:S128–S133Google Scholar
  68. 68.
    Queiroz DMM, Harris PR, Sanderson IR, Windle HJ, Walker MM, Rocha AMC, Rocha GA, Carvalho SD, Bittencourt PFS, de Castro LPF (2013) Iron status and Helicobacter pylori infection in symptomatic children: an international multi-centered study. PLoS One 8(7):e68833Google Scholar
  69. 69.
    Harris PR, Serrano CA, Villagrán A, Walker MM, Thomson M, Duarte I, Windle HJ, Crabtree JE (2013) Helicobacter pylori-associated hypochlorhydria in children, and development of iron deficiency. J Clin Pathol 66(4):343–347Google Scholar
  70. 70.
    Cardenas VM, Prieto-Jimenez CA, Mulla ZD, Rivera JO, Dominguez DC, Graham DY, Ortiz M (2011) Helicobacter pylori eradication and change in markers of iron stores among non–iron-deficient children in El Paso, Texas: an etiologic intervention study. J Pediatr Gastroenterol Nutr 52(3):326–332Google Scholar
  71. 71.
    Homan M, Hojsak I, Kolaček S (2012) Helicobacter pylori in pediatrics. Helicobacter 17:43–48Google Scholar
  72. 72.
    Kindermann A, Lopes AI (2009) Helicobacter pylori infection in pediatrics. Helicobacter 14:52–57Google Scholar
  73. 73.
    Thomas J, Dale A, Bunn J, Harding M, Coward W, Cole T, Weaver L (2004) Early Helicobacter pylori colonisation: the association with growth faltering in the Gambia. Arch Dis Child 89(12):1149–1154Google Scholar
  74. 74.
    Mera RM, Correa P, Fontham EE, Reina JC, Pradilla A, Alzate A, Bravo LE (2006) Effects of a new Helicobacter pylori infection on height and weight in Colombian children. Ann Epidemiol 16(5):347–351Google Scholar
  75. 75.
    Prentice A, Darboe M (2008) Growth and host-pathogen interactions. The window of opportunity: pre-pregnancy to 24 months of age. Karger Publishers 61:197–210Google Scholar
  76. 76.
    Soylu ÖB, Ozturk Y (2008) Helicobacter pylori infection: effect on malnutrition and growth failure in dyspeptic children. Eur J Pediatr 167(5):557–562Google Scholar
  77. 77.
    Cherian S, Forbes D, Sanfilippo F, Cook A, Burgner D (2009) Helicobacter pylori, helminth infections and growth: a cross-sectional study in a high prevalence population. Acta Paediatr 98(5):860–864Google Scholar
  78. 78.
    Ozen A, Furman A, Berber M, Karatepe HO, Mutlu N, Sarıçoban HE, Büyükgebiz B (2011) The effect of Helicobacter pylori and economic status on growth parameters and leptin, ghrelin, and insulin-like growth factor (IGF)-I concentrations in children. Helicobacter 16(1):55–65Google Scholar
  79. 79.
    Yang Y-J, Sheu B-S, Yang H-B, Lu C-C, Chuang C-C (2012) Eradication of Helicobacter pylori increases childhood growth and serum acylated ghrelin levels. World J Gastroenterol: WJG 18(21):2674Google Scholar
  80. 80.
    Wang Y, Bi Y, Zhang L, Wang C (2012) Is Helicobacter pylori infection associated with asthma risk? A meta-analysis based on 770 cases and 785 controls. Int J Med Sci 9(7):603Google Scholar
  81. 81.
    Karimi A, Fakhimi-Derakhshan K, Imanzadeh F, Rezaei M, Cavoshzadeh Z, Maham S (2013) Helicobacter pylori infection and pediatric asthma. Iran J Microbiol 5(2):132Google Scholar
  82. 82.
    Chen Y, Blaser MJ (2008) Helicobacter pylori colonization is inversely associated with childhood asthma. J Infect Dis 198(4):553–560Google Scholar
  83. 83.
    Ertem D (2013) Clinical practice: Helicobacter pylori infection in childhood. Eur J Pediatr 172(11):1427–1434Google Scholar
  84. 84.
    Kawakami E, Machado RS, Reber M, Patrício FRS (2002) 13C-urea breath test with infrared spectroscopy for diagnosing Helicobacter pylori infection in children and adolescents. J Pediatr Gastroenterol Nutr 35(1):39–43Google Scholar
  85. 85.
    Megraud F (2005) On behalf of the European pediatric task force on Helicobacter pylori comparison of non-invasive tests to detect Helicobacter pylori infection in children and adolescents results of a multicenter European study. J Pediatr 146:198–203Google Scholar
  86. 86.
    Leal YA, Flores LL, Fuentes-Pananá EM, Cedillo-Rivera R, Torres J (2011) 13C-urea breath test for the diagnosis of Helicobacter pylori infection in children: a systematic review and meta-analysis. Helicobacter 16(4):327–337Google Scholar
  87. 87.
    Drumm B, Koletzko S, Oderda G, pylori EPTFoH (2000) Helicobacter pylori infection in children: a consensus statement. J Pediatr Gastroenterol Nutr 30(2):207–213Google Scholar
  88. 88.
    Pathak C, Bhasin D, Khanduja K (2004) Urea breath test for Helicobacter pylori detection: present status. Trop Gastroenterol 25(4):156–161Google Scholar
  89. 89.
    Delvin EE, Brazier JL, Deslandres C, Alvarez F, Russo P, Seidman E (1999) Accuracy of the [13C]-urea breath test in diagnosing Helicobacter pylori gastritis in pediatric patients. J Pediatr Gastroenterol Nutr 28(1):59–62Google Scholar
  90. 90.
    Kato S, Ozawa K, Konno M, Tajiri H, Yoshimura N, Shimizu T, Fujisawa T, Abukawa D, Minoura T, Iinuma K (2002) Diagnostic accuracy of the 13 C-urea breath test for childhood Helicobacter pylori infection: a multicenter Japanese study. Am J Gastroenterol 97(7):1668Google Scholar
  91. 91.
    Ogata SK, Kawakami E, Patrício FRS, Pedroso MZ, Santos AM (2001) Evaluation of invasive and non-invasive methods for the diagnosis of Helicobacter pylori infection in symptomatic children and adolescents. Sao Paulo Med J 119(2):67–71Google Scholar
  92. 92.
    Jones NL, Sherman PM (2001) Approaching Helicobacter pylori infection in children: level I evidence at last and a word of caution. J Pediatr 139(5):622–623Google Scholar
  93. 93.
    Canete A, Abunají Y, Alvarez-Calatayud G, DeVicente M, González-Holguera JA, Leralta M, Pajares JM, Gisbert JP (2003) Breath test using a single 50-mg dose of 13C-urea to detect Helicobacter pylori infection in children. J Pediatr Gastroenterol Nutr 36(1):105–111Google Scholar
  94. 94.
    Elitsur Y, Yahav J (2005) Helicobacter pylori infection in pediatrics. Helicobacter 10:47–53Google Scholar
  95. 95.
    Koletzko S, Konstantopoulos N, Bosman D, Feydt-Schmidt A, Van der Ende A, Kalach N, Raymond J, Rüssmann H (2003) Evaluation of a novel monoclonal enzyme immunoassay for detection of Helicobacter pylori antigen in stool from children. Gut 52(6):804–806Google Scholar
  96. 96.
    Roggero P, Bonfiglio A, Luzzani S, Valadè A, Cataliotti E, Corno G, Garlaschi MC, Carissimi E, Mosca F, Carnelli V (2002) Helicobacter pylori stool antigen test: a method to confirm eradication in children. J Pediatr 140(6):775–777Google Scholar
  97. 97.
    van Doorn OJ, Bosman DK, van’t Hoff BW, Taminiau JA, Fibo J, van der Ende A (2001) Helicobacter pylori stool antigen test: a reliable non-invasive test for the diagnosis of Helicobacter pylori infection in children. Eur J Gastroenterol Hepatol 13(9):1061–1065Google Scholar
  98. 98.
    Yee Y, Yip K, Que T, Chang K, Li K, Lee C, Wong S, Lau S, Szeto M (2002) Efficacy of enzyme immunoassay for the detection of Helicobacter pylori antigens in frozen stool specimens: local validation. Aliment Pharmacol Ther 16(10):1739–1742Google Scholar
  99. 99.
    Raguza D, Machado RS, Ogata SK, Granato CFH, Patrício FRS, Kawakami E (2010) Validation of a monoclonal stool antigen test for diagnosing Helicobacter pylori infection in young children. J Pediatr Gastroenterol Nutr 50(4):400–403Google Scholar
  100. 100.
    Wu D-C, Wu I-C, Wang S-W, Lu C-Y, Ke H-L, Yuan S-SF, Wang Y-Y, Chang W-H, Wang T-E, Bair M-J (2006) Comparison of stool enzyme immunoassay and immunochromatographic method for detecting Helicobacter pylori antigens before and after eradication. Diagn Microbiol Infect Dis 56(4):373–378Google Scholar
  101. 101.
    Makristathis A, Barousch W, Pasching E, Binder C, Kuderna C, Apfalter P, Rotter ML, Hirschl AM (2000) Two enzyme immunoassays and PCR for detection ofHelicobacter pylori in stool specimens from pediatric patients before and after eradication therapy. J Clin Microbiol 38(10):3710–3714Google Scholar
  102. 102.
    Crone J, Gold BD (2004) Helicobacter pylori infection in pediatrics. Helicobacter 9:49–56Google Scholar
  103. 103.
    Asfeldt A, Løchen M-L, Straume B, Steigen S, Florholmen J, Goll R, Nestegard O, Paulssen E (2004) Accuracy of a monoclonal antibody-based stool antigen test in the diagnosis of Helicobacter pylori infection. Scand J Gastroenterol 39(11):1073–1077Google Scholar
  104. 104.
    Gatta L, Vakil N, Ricci C, Osborn JF, Tampieri A, Perna F, Miglioli M, Vaira D (2004) Effect of proton pump inhibitors and antacid therapy on 13 C urea breath tests and stool test for Helicobacter pylori infection. Am J Gastroenterol 99(5):823Google Scholar
  105. 105.
    Gisbert J, Trapero M, Calvet X, Mendoza J, Quesada M, Güell M, Pajares J (2004) Evaluation of three different tests for the detection of stool antigens to diagnose Helicobacter pylori infection in patients with upper gastrointestinal bleeding. Aliment Pharmacol Ther 19(8):923–929Google Scholar
  106. 106.
    Kuloğlu Z, Kansu A, Kırsaçlıoğlu CT, Üstündağ G, Aysev D, Ensari A, Küçük NÖ, Girgin N (2008) A rapid lateral flow stool antigen immunoassay and 14C-urea breath test for the diagnosis and eradication of Helicobacter pylori infection in children. Diagn Microbiol Infect Dis 62(4):351–356Google Scholar
  107. 107.
    Nares-Cisneros J, Jaramillo-Rodríguez Y, Martínez-Ordaz VA, Velasco-Rodríguez VM, Madero A, Mena-Arias G, Manriquez-Covarrubias L (2007) Immunochromatographic monoclonal test for detection of Helicobacter pylori antigen in stool is useful in children from high-prevalence developing country. Helicobacter 12(4):354–358Google Scholar
  108. 108.
    Yang HR, Seo JK (2008) Helicobacter pylori stool antigen (HpSA) tests in children before and after eradication therapy: comparison of rapid immunochromatographic assay and HpSA ELISA. Dig Dis Sci 53(8):2053–2058Google Scholar
  109. 109.
    Choi J, Kim CH, Kim D, Chung SJ, Song JH, Kang JM, Yang JI, Park MJ, Kim YS, Yim JY (2011) Prospective evaluation of a new stool antigen test for the detection of Helicobacter pylori, in comparison with histology, rapid urease test, 13C-urea breath test, and serology. J Gastroenterol Hepatol 26(6):1053–1059Google Scholar
  110. 110.
    Day AS, Sherman PM (2002) Accuracy of office-based immunoassays for the diagnosis of Helicobacter pylori infection in children. Helicobacter 7(3):205–209Google Scholar
  111. 111.
    Guarner J, Kalach N, Elitsur Y, Koletzko S (2010) Helicobacter pylori diagnostic tests in children: review of the literature from 1999 to 2009. Eur J Pediatr 169(1):15–25Google Scholar
  112. 112.
    Czinn SJ (1999) Serodiagnosis of Helicobacter pylori in pediatric patients. LWWGoogle Scholar
  113. 113.
    Daugule I, Rowland M (2008) Helicobacter pylori infection in children. Helicobacter 13:41–46Google Scholar
  114. 114.
    Westblom T, Madan E, Gudipati S, Midkiff B, Czinn S (1992) Diagnosis of Helicobacter pylori infection in adult and pediatric patients by using Pyloriset, a rapid latex agglutination test. J Clin Microbiol 30(1):96–98Google Scholar
  115. 115.
    Kato S, Nakayama K, Minoura T, Konno M, Tajiri H, Matsuhisa T, Iinuma K (2004) Comparison between the 13 C-urea breath test and stool antigen test for the diagnosis of childhood Helicobacter pylori infection. J Gastroenterol 39(11):1045–1050Google Scholar
  116. 116.
    Hino B, Eliakim R, Levine A, Sprecher H, Berkowitz D, Hartman C, Eshach-Adiv O, Shamir R (2004) Comparison of invasive and non-invasive tests diagnosis and monitoring of Helicobacter pylori infection in children. J Pediatr Gastroenterol Nutr 39(5):519–523Google Scholar
  117. 117.
    Thijs J, Van Zwet A, Thijs W, Oey H, Karrenbeld A, Stellaard F, Luijt D, Meyer B, Kleibeuker J (1996) Diagnostic tests for Helicobacter pylori: a prospective evaluation of their accuracy, without selecting a single test as the gold standard. Am J Gastroenterol 91(10):2125–2129Google Scholar
  118. 118.
    Dixon MF, Genta RM, Yardley JH, Correa P (1996) Classification and grading of gastritis: the updated Sydney system. Am J Surg Pathol 20(10):1161–1181Google Scholar
  119. 119.
    Malfertheiner P, Megraud F, O'morain CA, Atherton J, Axon AT, Bazzoli F, Gensini GF, Gisbert JP, Graham DY, Rokkas T (2012) Management of Helicobacter pylori infection—the Maastricht IV/Florence consensus report. Gut 61(5):646–664Google Scholar
  120. 120.
    Garza-González E, Perez-Perez GI, Maldonado-Garza HJ, Bosques-Padilla FJ (2014) A review of Helicobacter pylori diagnosis, treatment, and methods to detect eradication. World J Gastroenterol: WJG 20(6):1438Google Scholar
  121. 121.
    Gold BD, Colletti RB, Abbott M, Czinn SJ, Elitsur Y, Hassall E, Macarthur C, Snyder J, Sherman PM (2000) Helicobacter pylori infection in children: recommendations for diagnosis and treatment. J Pediatr Gastroenterol Nutr 31(5):490–497Google Scholar
  122. 122.
    Sabbi T, De Angelis P, Colistro F, Dall’Oglio L, di Abriola GF, Castro M (2005) Efficacy of noninvasive tests in the diagnosis of Helicobacter pylori infection in pediatric patients. Arch Pediatr Adolesc Med 159(3):238–241Google Scholar
  123. 123.
    Madani S, Rabah R, Tolia V (2000) Diagnosis of Helicobacter pylori infection from antral biopsies in pediatric patients: is urease test that reliable? Dig Dis Sci 45(6):1233–1237Google Scholar
  124. 124.
    Ni Y-H, Lin J-T, Huang S-F, Yang J-C, Chang M-H (2000) Accurate diagnosis Helicobacter pylori infection by stool antigen test and 6 other currently available tests in children. J Pediatr 136(6):823–827Google Scholar
  125. 125.
    Velapatino B, Balqui J, Gilman RH, Bussalleu A, Quino W, Finger SA, Santivanez L, Herrera P, Piscoya A, Valdivia J (2006) Validation of string test for diagnosis of Helicobacter pylori infections. J Clin Microbiol 44(3):976–980Google Scholar
  126. 126.
    Belda S, Saez J, Santibáñez M, Rodríguez JC, Galiana A, Sola-Vera J, Ruiz-García M, Brotons A, López-Girona E, Girona E (2012) Quantification of Helicobacter pylori in gastric mucosa by real-time polymerase chain reaction: comparison with traditional diagnostic methods. Diagn Microbiol Infect Dis 74(3):248–252Google Scholar
  127. 127.
    Molnar B, Szoke D, Ruzsovics A, Tulassay Z (2008) Significantly elevated Helicobacter pylori density and different genotype distribution in erosions as compared with normal gastric biopsy specimen detected by quantitative real-time PCR. Eur J Gastroenterol Hepatol 20(4):305–313Google Scholar
  128. 128.
    Rimbara E, Sasatsu M, Graham DY (2013) PCR detection of Helicobacter pylori in clinical samples. Methods Mol Biol 943:279–87Google Scholar
  129. 129.
    Duś I, Dobosz T, Manzin A, Loi G, Serra C, Radwan-Oczko M (2013) Role of PCR in Helicobacter pylori diagnostics and research‐‐new approaches for study of coccoid and spiral forms of the bacteria. Postepy Hig Med Dosw (Online) 67(9):261–218Google Scholar
  130. 130.
    Kalach N, Gosset P, Dehecq E, Decoster A, Spyckerelle C, Papadopolos S, Dupont C, Raymond J (2015) Usefulness of gastric biopsy–based real-time polymerase chain reaction for the diagnosis of Helicobacter pylori infection in children. J Pediatr Gastroenterol Nutr 61(3):307–312Google Scholar
  131. 131.
    Chung WC, Jung SH, Oh JH, Kim TH, Cheung DY, Kim BW, Kim SS, Kim JI, Sin EY (2014) Dual-priming oligonucleotide-based multiplex PCR using tissue samples in rapid urease test in the detection of Helicobacter pylori infection. World J Gastroenterol: WJG 20(21):6547Google Scholar
  132. 132.
    Bazin T, Nchare Mfondi A, Julie C, Émile J-F, Raymond J, Lamarque D (2018) Contribution of genetic amplification by PCR for the diagnosis of Helicobacter pylori infection in patients receiving proton pump inhibitors. United European Gastroenterol J 6(8):1267–1273Google Scholar
  133. 133.
    Yakoob J, Jafri W, Abbas Z, Abid S, Islam M, Ahmed Z (2008) The diagnostic yield of various tests for Helicobacter pylori infection in patients on acid-reducing drugs. Dig Dis Sci 53(1):95–100Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Parisa Sabbagh
    • 1
  • Mostafa Javanian
    • 1
  • Veerendra Koppolu
    • 2
  • VeneelaKrishna Rekha Vasigala
    • 3
  • Soheil Ebrahimpour
    • 1
    Email author
  1. 1.Infectious Diseases and Tropical Medicine Research Center, Health Research InstituteBabol University of Medical SciencesBabolIslamic Republic of Iran
  2. 2.Scientist Biopharmaceutical Development Medimmune GaithersburgGaithersburgUSA
  3. 3.Rangaraya Medical CollegeNTR University of Health SciencesKakinadaIndia

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