Advertisement

Epidemiology, Diagnosis and Risk Factors of Helicobacter pylori Infection

  • Kallirroi Kotilea
  • Patrick Bontems
  • Eliette TouatiEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1149)

Abstract

Helicobacter pylori is a human-specific pathogen, which leads to gastric pathologies including gastric cancer. It is a highly unique bacterium considered as a carcinogenic agent. H. pylori remains a major human health problem, responsible for ~90% of the gastric cancer cases. Approximately four billion individuals have been detected for H. pylori infection worldwide in 2015. At the turn of the twenty-first century, the prevalence of H. pylori has been declining in highly industrialized countries of the Western world, whereas prevalence has plateaued at a high level in developing and newly industrialized countries. However, the infection status remains high in immigrants coming from countries with high prevalence of H. pylori infection. H. pylori can be diagnosed both by invasive and non-invasive methods. Urea breath test and stool antigens detection are among the most commonly used non-invasive ones. Although the way H. pylori is transmitted remains still not fully clear, the level of contamination is strongly dependent on the familial and environmental context, with a drastic impact of living conditions with poor hygiene and sanitation. However, familial socioeconomic status is the main risk factor for H. pylori infection among children. In addition, food and water source have a high impact on the prevalence of H. pylori infection worldwide. This chapter highlights the latest knowledge in the epidemiology of H. pylori infection, its diagnosis and critical risk factors responsible for its high prevalence in some populations and geographic areas.

Keywords

Prevalence Invasive and non-invasive methods Familial factors Environment Life habits 

References

  1. Abdul Rahim NR, Benson J, Grocke K, Vather D, Zimmerman J, Moody T, Mwanri L (2017) Prevalence of Helicobacter pylori infection in newly arrived refugees attending the Migrant Health Service, South Australia. Helicobacter 22(2).  https://doi.org/10.1111/hel.12360
  2. Adams BL, Bates TC, Oliver JD (2003) Helicobacter pylori in a natural freshwater environment. Appl Environ Microbiol 69(12):7462–7466.  https://doi.org/10.1128/AEM.69.12.7462-7466.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  3. Aguemon BD, Struelens MJ, Massougbodji OEM (2005) Prevalence and risk-factors for Helicobacter pylori infection in urban and rural Beninese populations. Clin Microbiol Infect 11(8):611–617.  https://doi.org/10.1111/j.1469-0691.2005.01189.x CrossRefGoogle Scholar
  4. Aguilera-Correa JJ, Urruzuno P, Barrio J, Martinez MJ, Agudo S, Somodevilla A, Liorca L, Alarcon T (2017) Detection of Helicobacter pylori and the genotypes of resistance to clarithromycin and the heterogeneous genotype to this antibiotic in biopsies obtained from symptomatic children. Diag Microbiol Infect Dis 87(2):150–153.  https://doi.org/10.1016/j.diagmicrobio.2016.03.001 CrossRefGoogle Scholar
  5. Ahn J, Sinha R, Pei Z, Dominianni C, Wu J, Shi J, Goedert IJ, Hayes RB, Yang L (2013) Human gut microbiome and risk for colorectal cancer. J Natl Cancer Inst 105(24):1907–1911.  https://doi.org/10.1093/jnci/djt300 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Amaral O, Fernandes I, Veiga N, Pereira C, Chaves C, Nelas P, Silva D (2017) Living conditions and Helicobacter pylori in adults. Biomed Res Int 2017:9082716.  https://doi.org/10.1155/2017/9082716 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Andersen LP, Wewer AV, Christiansen KM, Tvede M, Hansen JP, Henriksen FW, Krasilnikoff PA (1994) The humoral immune response to Helicobacter pylori infection in children with recurrent abdominal pain. APMIS 102(6):457–464CrossRefGoogle Scholar
  8. Angelidis AS, Tirodimos I, Bobos M, Kalamaki MS, Papageorgiou DK, Arvanitidou M (2011) Detection of Helicobacter pylori in raw bovine milk by fluorescence in situ hybridization (FISH). Int J Food Microbiol 151(2):252–256.  https://doi.org/10.1016/j.ijfoodmicro.2011.09.007 CrossRefGoogle Scholar
  9. Arnold IC, Dehzad N, Reuter S, Martin H, Becher B, Taube C, Müller A (2011) Helicobacter pylori infection prevents allergic asthma in mouse models through the induction of regulatory T cells. J Clin Invest 121:3088–3093.  https://doi.org/10.1172/JCI45041 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Asgeirsdottir GA, Kjartansdottir I, Olafsdottir AS, Hreinsson JP, Hrafnkelsson H, Johannsson E, Björnsson ES (2017) Helicobacter pylori infection in Icelandic children. Scand J Gastroenterol 52(6-7):686–690.  https://doi.org/10.1080/00365521.2017.1304986 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Assaad S, Chaaban R, Tannous F, Costanian C (2018) Dietary habits and Helicobacter pylori infection: a cross sectional study at a Lebanese hospital. BMC Gastroenterol 18(1):48.  https://doi.org/10.1186/s12876-018-0775-1 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Azevedo NF, Almeida C, Fernandes I, Cerqueira L, Dias S, Keevil CW, Vieira JM (2008) Survival of gastric and enterohepatic helicobacter spp. in water. implications for transmission. Appl Environ Microbiol 74(6):1805–1811.  https://doi.org/10.1128/AEM.02241-07 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Aziz RK, Khalifa MM, Sharaf RR (2015) Contaminated water as a source of Helicobacter pylori infection : a review. J Adv Res 6:539–547.  https://doi.org/10.1016/j.jare.2013.07.007 CrossRefGoogle Scholar
  14. Bastos J, Peleteiro B, Pinto H, Marinho A, Guimaraes JT, Ramos E, La Vecchia C, Barros H, Lunet N (2013) Prevalence, incidence and risk factors for Helicobacter pylori infection in a cohort of Portuguese adolescents (EpiTeen). Dig Liver Dis 45(4):290–295.  https://doi.org/10.1016/j.dld.2012.11.009 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Best LM, Takwoingi Y, Siddique S, Selladurai A, Gandhi A, Low B, Yaghoobi M, Gurusamy KS (2018) Non-invasive diagnostic tests for Helicobacter pylori infection. Cochren Database Syst Rev 3:CD012080.  https://doi.org/10.1002/14651858.CD012080.pub2 CrossRefGoogle Scholar
  16. Biernat MM, Iwanczak B, Binkowska A, Grabinska J, Gosciniak G (2016) The prevalence of Helicobacter pylori infection in symptomatic children: a 13-year observational study in the lower Silesian region. Adv Clin Exp Med 25(2):303–308.  https://doi.org/10.17219/acem/44372 CrossRefGoogle Scholar
  17. Boehnke KF, Eaton KA, Valdivieso M, Baker LH, Xi C (2015) Animal model reveals potential waterborne transmission of Helicobacter pylori infection. Helicobacter 20(5):326–333.  https://doi.org/10.1111/hel.12216 CrossRefGoogle Scholar
  18. Boehnke KF, Eaton KA, Fontaine C, Brewster R, Wu J, Eisenberg JNS, Valdivieso M, Baker LH, Xi C (2017) Reduced infectivity of waterborne viable but nonculturable Helicobacter pylori strain SS1 in mice. Helicobacter 22(4).  https://doi.org/10.1111/hel.12391
  19. Bontems P, Devaster JM, Corvaglia L, Dezsöfi A, Van Den Borre C, Goutier S, Butzler JP, Cadranel S (2001) Twelve year observation of primary and secondary antibiotic-resistant Helicobacter pylori strains in children. Pediatr Infect Dis J 20(11):1033–1038CrossRefGoogle Scholar
  20. Burucoa C, Delchier JC, Courillon-Mallet A, de Korwin JD, Mégraud F, Zerbib F, Raymond J, Fauchère JL (2013) Comparative evaluation of 29 commercial Helicobacter pylori serological kits. Helicobacter 18(3):169–179.  https://doi.org/10.1111/hel.12030 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Cadranel S, Corvaglia L, Bontems P, Deprez C, Glupczynski Y, Van Riet A, Keppens E (1998) Detection of Helicobacter pylori infection in children with a standardized and simplified 13C-urea breath test. J Pediatr Gastroenterol Nutr 27(3):275–280CrossRefPubMedPubMedCentralGoogle Scholar
  22. Capelle LG, De Vries AC, Haringsma J, Ter Borg F, de Vries RA, Bruno MJ, van Dekken H, Meijer J, van Grieken NC, Kuipers EJ (2010) The staging of gastritis with the OLGA system by using intestinal metaplasia as an accurate alternative for atrophic gastritis. Gastrointest Endosc 71(7):1150–1158.  https://doi.org/10.1016/j.gie.2009.12.029 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Cardenas VM, Mulla ZD, Ortiz M, Graham DY (2006) Iron deficiency and Helicobacter pylori infection in the United States. Am J Epidemiol 163(2):127–134.  https://doi.org/10.1093/aje/kwj018 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Carreira H, Bastos A, Peleteiro B, Lunet N (2015) Breast-feeding and Helicobacter pylori infection: systematic review and meta-analysis. Public Health Nutr 18(3):500–520.  https://doi.org/10.1017/S1368980014000500 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Chan FT, Mackenzie AM (1986) Evaluation of primary selective media and enrichment methods for Campylobacter species isolation. Eur J Clin Microbiol 5(2):162–164CrossRefPubMedPubMedCentralGoogle Scholar
  26. Correa P (1992) Human gastric carcinogenesis: a multistep and multifactorial process. First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res 52(24):6735–6740PubMedGoogle Scholar
  27. Correa P, Piazuelo MB (2011) Helicobacter pylori infection and gastric adenocarcinoma. US. Gastroenterol Hepatol Rev 7(1):59–64Google Scholar
  28. Corvaglia L, Bontems P, Devaster JM, Heimann P, Glupczynski Y, Keppens E, Cadranel S (1999) Accuracy of serology and 13C-urea breath test for detection of Helicobacter pylori in children. Pediatr Infect Dis J 18(11):976–979CrossRefPubMedPubMedCentralGoogle Scholar
  29. Daugule I, Karklina D, Rudzite D, Remberga S, Rumba-Rozenfelde I (2016) Prevalence of Helicobacter pylori infection among preschool children in Latvia: no significant decrease in prevalence during a ten year period. Scand J Public Health 44(4):418–422.  https://doi.org/10.1177/1403494816631861 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Dixon MF, Genta RM, Yardley JH, Correa P (1996) Classification and grading of gastritis. The updated Sydney System. International Workshop on the Histopathology of Gastritis, Houston 1994. Am J Surg Pathol 20(10):1161–1181CrossRefGoogle Scholar
  31. Dore MP, Bilotta M, Vaira D, Manca A, Massarelli G, Leandro G, Atzei A, Pisanu G, Graham DY, Realdi G (1999a) High prevalence of Helicobacter pylori infection in shepherds. Dig Dis Sci 44(6):1161–1164CrossRefGoogle Scholar
  32. Dore MP, Sepulveda AR, Osato MS, Realdi G, Graham DY (1999b) Helicobacter pylori in sheep milk. Lancet 354(9173):132.  https://doi.org/10.1016/S0140-6736(99)01724-9 CrossRefGoogle Scholar
  33. Dore MP, Sepulveda AR, Al-Zimaity H, Yamaoka Y, Osato MS, Mototsugu K, Nieddu AM, Realdi G, Graham DY (2001) Isolation of Helicobacter pylori from sheep-implications for transmission to humans. Am J Gastroenterol 96(5):1396–1401.  https://doi.org/10.1111/j.1572-0241.2001.03772.x CrossRefPubMedGoogle Scholar
  34. Dore MP, Malaty HM, Graham DY, Fanciulli G, Delitalia G, Realdi G (2002) Risk Factors Associated with Helicobacter pylori infection among children in a defined geographic area. Clin Infect Dis 35(3):240–245.  https://doi.org/10.1086/341415 CrossRefGoogle Scholar
  35. Douraghi M, Nateghi Rostami M, Goudarzi H, Ghalavand Z (2013) Comparison of stool antigen immunoassay and serology for screening for Helicobacter pylori infection in intellectually disabled children. Microbiol Immunol 57(11):772–777.  https://doi.org/10.1111/1348-0421.12099 CrossRefGoogle Scholar
  36. Eslick GD, Lim LL, Byles JE, Xia HH, Talley NJ (1999) Association of Helicobacter pylori infection with gastric carcinoma: a meta-analysis. Am J Gastroenterol 94(9): 2373-2379.  https://doi.org/10.1111/j.1572-0241.1999.01360.x
  37. Everhart JE, Kruszon-Moran D, Perez-Perez GI, Tralka TS, McQuillan G (2000) Seroprevalence and ethnic differences in Helicobacter pylori infection among adults in the United States. J Infect Dis 181:1359–1363.  https://doi.org/10.1086/315384 CrossRefGoogle Scholar
  38. Fallone CA, Chiba N, Van Zanten S, Fischbach L, Gisbert JP, Hunt RH, Jones NL, Render C, Leontiadis GI, Moayyedi P, Marshall JK (2016) The Toronto consensus for the treatment of Helicobacter pylori Infection in Adults. Gastroenterology 151(1):51–69.  https://doi.org/10.1053/j.gastro.2016.04.006 CrossRefGoogle Scholar
  39. Fernandes RM, Silva H, Oliveira R, Almeida C, Azevedo NF, Vieira MJ (2017) Morphological transition of Helicobacter pylori adapted to water. Future Microbiol 12(13):1167–1179.  https://doi.org/10.2217/fmb-2016-0174 CrossRefGoogle Scholar
  40. Ferreira RM, Pereira-Marques J, Pinto-Ribeiro I, Costa JL, Carneiro F, Machado JC, Figueiredo C (2018) Gastric microbial community profiling reveals a dysbiotic cancer associated microbiota. Gut 67(2):226–236.  https://doi.org/10.1136/gutjnl-2017-314205 CrossRefGoogle Scholar
  41. Fujimura S, Kawamura T, Kato S, Tateno H, Watanabe A (2002) Detection of Helicobacter pylori in cow’s milk. Lett Appl Microbiol 35(6):504–507.  https://doi.org/10.1046/j.1472-765X.2002.01229.x CrossRefGoogle Scholar
  42. Fujimura S, Kato S, Watanabe A (2008) Water source as a Helicobacter pylori transmission route: a 3-year follow-up study of Japanese children living in a unique district. J Med Microbiol 57(Pt 7):909–910.  https://doi.org/10.1099/jmm.0.47683-0 CrossRefPubMedGoogle Scholar
  43. Garcia A, Salas-Jara MJ, Herrera C, Gonzalez C (2014) Biofilm and Helicobacter pylori: from environment to human host. World J Gastroenterol 20(19):5632–5638.  https://doi.org/10.3748/wjg.v20.i19.5632 CrossRefPubMedPubMedCentralGoogle Scholar
  44. Gevers D, Kugathasan S, Denson LA, Vazquez-Baeza Y, Van Treuren W, Ren B, Schwager E, Knights D, Song SJ, Yassour M, Morgan XC, Kostic AD, Luo C, Gonzalez A, McDonald D, Haberman Y, Walters T, Baker S, Rosh J, Stephens M, Heyman M, Markowitz J, Baldassano R, Griffiths A, Sylvester F, Mack D, Kim S, Crandall W, Hyams J, Huttenhower C, Knight R, Xavier RJ (2014) The treatment-naive microbiome in new onset Crohn’s disease. Cell Host Microbe 15(3):382–392.  https://doi.org/10.1016/j.chom.2014.02.005 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Goodman KJ, Correa P (2000) Transmission of Helicobacter pylori among siblings. Lancet 355(9201):358–362.  https://doi.org/10.1016/S0140-6736(99)05273-3 CrossRefGoogle Scholar
  46. Goodman KJ, Correa P, Tengana Aux HJ, Ramirez H, DeLany JP, Guerrero Pepinosa O, Lopez Quinones M, Collazos Parra T (1996) Helicobacter pylori infection in the Colombian Andes: a population-based study of transmission pathways. Am J Epidemiol 144(3):290–299CrossRefGoogle Scholar
  47. Goodman KJ, Correa P, Tengana Aux HJ, DeLany JP, Collazos T (1997) Nutritional factors and Helicobacter pylori infection in Colombian children. J Pediatr Gastroenterol Nutr 25(5):507–515CrossRefGoogle Scholar
  48. Graham DY, Klein PD, Evans DJ Jr, Evans DG, Alpert LC, Opekun AR, Boutton TW (1987) Campylobacter pylori detected noninvasively by the 13C-urea breath test. Lancet 1(8543):1174–1177.  https://doi.org/10.1016/S0140-6736(87)92145-3 CrossRefGoogle Scholar
  49. Graham DY, Lu H, Yamaoka Y (2009) African, Asian or Indian enigma, the East Asian Helicobacter pylori: facts or medical myths. J Dig Dis 10(2):77–84.  https://doi.org/10.1111/j.1751-2980.2009.00368.x CrossRefPubMedPubMedCentralGoogle Scholar
  50. 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):15-25.  https://doi.org/10.1007/s00431-009-1033-x
  51. Hamrah MH, Hamrah MS, Hassan Hamrah M, Kanda M, Hamrah AE, Dahi AE, Homayoun F, Hamrah MH, Fotouhi A, Sakamoto J (2017) Prevalence of Helicobacter pylori infection in dyspeptic patients in Andkhoy Afghanistan. Asian Pac J Cancer Prev 18(11):3123–3127.  https://doi.org/10.22034/APJCP.2017.18.11.3123 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Hasosah M, Satti M, Shehzad A, Alsahafi A, Sukkar G, Alzaben A, Sunaid A, Ahmed A, AlThubiti S, Mufti A, Jacobson K (2015) Prevalence and risk factors of Helicobacter pylori infection in Saudi children: a three-year prospective controlled study. Helicobacter 20(1):56–63.  https://doi.org/10.1111/hel.12172 CrossRefGoogle Scholar
  53. Honar N, Minazadeh A, Shakibazad N, Haghighat M, Saki F, Javaherizadeh H (2016) Dagnostic accuracy of urea breath breath test for Helicobacter pylori infection in children with dyspepsia in comparison to histopathology. Arq Gastroenterol 53(2):108–112.  https://doi.org/10.1590/S0004-28032016000200011 CrossRefPubMedPubMedCentralGoogle Scholar
  54. Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D, Malfertheimer P, Graham DY, Wong VWS, Wu JCY, Chan FKL, Sung JJY, Kaplan GG, Ng SC (2017) Global prevalence of Helicobacter pylori infection: systematic review and meta-analysis. Gastroenterology 153(2):420–429.  https://doi.org/10.1053/j.gastro.2017.04.022 CrossRefGoogle Scholar
  55. Horiuchi T, Ohkusa T, Watanabe M, Kobayashi D, Miwa H, Eishi Y (2001) Helicobacter pylori DNA in drinking water in Japan. Microbiol Immunol 45(7):515–519.  https://doi.org/10.1111/j.1348-0421.2001.tb02652.x CrossRefGoogle Scholar
  56. Hulten K, Hans SW, Enroth H, Klein PD, Opekun AR, Gilman RH, Evans DG, Engstrand L, Graham DY, El-Zaatari FA (1996) Helicobacter pylori in the drinking water in Peru. Gastroenterology 110(4):1031–1035.  https://doi.org/10.1053/gast.1996.v110.pm8612990 CrossRefGoogle Scholar
  57. IARC (1994) Schistosomes, liver flukes and Helicobacter pylori. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Lyon, 7–14 June 1994. IARC Monogr Eval Carcinog Risks Hum 61:1–241Google Scholar
  58. Jones NL, Koletzko S, Goodman K, Bontems P, Cadranel S, Casswall T, Czinn S, Gold BD, Guarner J, Elitsur Y, Homan M, Kalach N, Kori M, Madrazo A, Mégraud F, Papadopoulo A, Rowland M, ESPGHAN NASPGHAN (2017) Joint ESPGHAN/NASPGHAN Guidelines for the Management of Helicobacter pylori in Children and Adolescents (Update 2016). J Pediatr Gastroenterol Nutr 64(6):991–1003.  https://doi.org/10.1097/MPG.0000000000001594 CrossRefPubMedPubMedCentralGoogle Scholar
  59. 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):307–312.  https://doi.org/10.1097/MPG.0000000000000787 CrossRefGoogle Scholar
  60. Kalach N, Gosset P, Dehecq E, Decoster A, Georgel AF, Spyckerelle C, Papadopoulo A, Dupont C, Raymond J (2017) A one-step immune-chromatographic Helicobacter pylori stool antigen test for children was quick, consistent, reliable and specific. Acta Paediatr 106(12):2025–2030.  https://doi.org/10.1111/apa.13968 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Kienesberger S, Cox LM, Livanos A, Zhang XS, Chung J, Perez-Perez G, Gorkiewicz G, Zechner EL, Blaser MJ (2016) Gastric Helicobacter pylori infection affects local and distant microbial populations and host responses. Cell Reports 14:1395–1407.  https://doi.org/10.1016/j.celrep.2016.01.017 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Kikuchi S, Kurosawa M, Sakiyama T (1998) Helicobacter pylori risk associated with sibship size and family history of gastric diseases in Japanese adults. Jpn J Cancer Res 89(11):1109-1112.  https://doi.org/10.1111/j.1349-7006.1998.tb00504.x
  63. Kodaman N, Pazos A, Schneider BG, Piazuelo MB, Mera R, Sobota RS, Sicinschi LA, Shaffer CL, Romero-Gallo J, de Sablet T, Harder RH, Bravo LE, Peek RM Jr, Wilson KT, Cover TL, Williams SM, Correa P (2014) Human and Helicobacter pylori coevolution shapes the risk of gastric disease. Proc Natl Acad Sci U S A 111(4):1455–1460.  https://doi.org/10.1073/pnas.1318093111 CrossRefPubMedPubMedCentralGoogle Scholar
  64. Koletzko S, Richy F, Bontems P, Crone J, Kalach N, Monteiro ML, Gottrand F, Celinska-Cedro D, Roma-Giannikou E, Orderda G, Kolacek S, Urruzuno P, Martinez-Gomez MJ, Casswall T, Ashorn M, Bodanszky H, Mégraud F (2006) Prospective multicentre study on antibiotic resistance of Helicobacter pylori strains obtained from children living in Europe. Gut 55(12):1711–1716.  https://doi.org/10.1136/gut.2006.091272 CrossRefPubMedPubMedCentralGoogle Scholar
  65. Kusano C, Gotoda T, Ishikawa MM (2017) The administrative project of Helicobacter pylori infection screening among junior high school students in an area of Japan with a high incidence of gastric cancer. Gastric Cancer 20(Suppl 1):16–19.  https://doi.org/10.1007/s10120-017-0688-7 CrossRefPubMedPubMedCentralGoogle Scholar
  66. Lash RH, Genta RM (2016) Routine Anti-Helicobacter immunohistochemical staining is significantly superior to reflex staining protocols for the detection of Helicobacter in gastric biopsy specimens. Helicobacter 21(6):581–585.  https://doi.org/10.1111/hel.12315 CrossRefPubMedPubMedCentralGoogle Scholar
  67. Leal YA, Flores LL, Fuentes-Panana 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):327–337.  https://doi.org/10.1111/j.1523-5378.2011.00863.x CrossRefGoogle Scholar
  68. Makristathis A, Pasching E, Schutze K, Wimmer M, Rotter ML, Hirschl AM (1998) Detection of Helicobacter pylori in stool specimens by PCR and antigen enzyme immunoassay. J Clin Microbiol 36(9):2772–2774PubMedPubMedCentralGoogle Scholar
  69. Malaty HM, Evans DG, Evans DJ Jr, Graham DY (1992) Helicobacter pylori in Hispanics: comparison with blacks and whites of similar age and socioeconomic class. Gastroenterology 103(3):813–816.  https://doi.org/10.1016/0016-5085(92)90011-M CrossRefPubMedPubMedCentralGoogle Scholar
  70. Malfertheiner P, Mégraud F, O’Morain CA, Gisbert JP, Kuipers EJ, Axon AT, Bazzoli F, Gasbarrini A, Atherton J, Graham DY, Hunt R, Moayyedi P, Rokkas T, Rugge M, Selgrad M, Suerbaum S, Sugano K, El-Omar EM, European Helicobacter and Microbiota Study Group and Consensus Panel (2017) Management of Helicobacter pylori infection-the Maastricht V/Florence consensus report. Gut 66(1):6–30.  https://doi.org/10.1136/gutjnl-2016-312288 CrossRefPubMedPubMedCentralGoogle Scholar
  71. Mana F, Vandebosch S, Miendje Deyi V, Haentjens P, Urbain D (2013) Prevalence of and risk factors for H. pylori infection in healthy children and young adults in Belgium anno 2010/2011. Acta Gastroenterol Belg 76(4):381–385PubMedGoogle Scholar
  72. Mastromarino P, Conti C, Donato K, Strappini PM, Cattaruzza MS, Orsi GB (2005) Does hospital work constitute a risk factor for Helicobacter pylori infection? J Hosp Infect 60:261–268.  https://doi.org/10.1016/j.jhin.2004.12.019 CrossRefGoogle Scholar
  73. McNulty CA, Wise R (1985) Rapid diagnosis of Campylobacter-associated gastritis. Lancet 1(8443):1443–1444.  https://doi.org/10.1016/S0140-6736(85)91865-3 CrossRefGoogle Scholar
  74. Mendall MA, Goggin PM, Molineaux N, Levy J, Toosy T, Strachan D, Northfield TC (1992) Childhood living conditions and Helicobacter pylori seropositivity in adult life. Lancet 339:896–897.  https://doi.org/10.1016/0140-6736(92)90931-R CrossRefGoogle Scholar
  75. Miendje Deyi VY, Bontems P, Vanderpas J, De Koster E, Nitounda R, Van den Borre C, Cadranel S, Burette A (2011) Multicenter survey of routine determinations of resistance of Helicobacter pylori to antimicrobials over the last 20 years (1990 to 2009) in Belgium. J Clin Microbiol 49(6):2200–2209.  https://doi.org/10.1128/JCM.02642-10 CrossRefPubMedPubMedCentralGoogle Scholar
  76. Moayyedi P, Soo S, Deeks J, Delaney B, Harris A, Innes M, Oakes R, Wilson S, Roalfe A, Bennett C, Forman D (2006) Eradication of Helicobacter pylori for non-ulcer dyspepsia. Cochrane Database Syst Rev (19, 2):Cd002096.  https://doi.org/10.1002/14651858.CD002096.pub4
  77. Momtaz H, Dabiri H, Souod N, Gholami M (2014) Study of Helicobacter pylori genotype status in cows, sheep, goats and human beings. BMC Gastroenterol 14(61).  https://doi.org/10.1186/1471-230X-14-61
  78. Moosazadeh M, Lankarani KB, Afshari M (2016) Meta-analysis of the prevalence of Helicobacter pylori infection among children and adults of Iran. Int J Prev Med 7:48.  https://doi.org/10.4103/2008-7802.177893 CrossRefPubMedPubMedCentralGoogle Scholar
  79. Morais S, Costa AR, Ferro A, Lunet N, Peleteiro B (2017) Contemporary migration patterns in the prevalence of Helicobacter pylori infection: a systematic review. Helicobacter 22(3).  https://doi.org/10.1111/hel.12372
  80. Moreno Y, Ferrus MA (2012) Specific detection of cultivable Helicobacter pylori cells from wastewater treatment plants. Helicobacter 17(5):327–332.  https://doi.org/10.1111/j.15235378.2012.00961.x CrossRefGoogle Scholar
  81. Mousavi S, Dehkordi FS, Rahimi E (2014) Virulence factors and antibiotic resistance of Helicobacter pylori isolated from raw milk and unpasteurized dairy products in Iran. J Venom Anim Toxins Incl Trop Dis 20:51.  https://doi.org/10.1186/1678-9199-20-51 CrossRefPubMedPubMedCentralGoogle Scholar
  82. Murray LJ, McCrum EE, Evans AE, Bamford KB (1997) Epidemiology of Helicobacter pylori infection among 4742 randomly selected subjects from Northern Ireland. Int J Epidemiol 26:880–887CrossRefGoogle Scholar
  83. Nakayama Y, Lin Y, Hongo M, Hidaka H, Kikuchi S (2017) Helicobacter pylori infection and its related factors in junior high school students in Nagano Prefecture, Japan. Helicobacter 22(2).  https://doi.org/10.1111/hel.12363
  84. Nguyen TVH, Nguyen VB, Binh Phan TT et al (2016) Epidemiology of Helicobacter pylori infection in Tay Children in Vietnam. Ann Clin Lab Res 04:1–9. Available from: http://www.aclr.com.es/clinical-research/epidemiology-of-helicobacter-pylori-infection-in-tay-children-in-vietnam.pH. pylori?aid=17244
  85. Ogihara A, Kikuchi S, Hasegawa A, Kurosawa M, Miki K, Kaneko E, Mizukoshi H (2000) Relationship between Helicobacter pylori infection and smoking and drinking habits. J Gastroenterol Hepatol 15(3):271–276CrossRefGoogle Scholar
  86. Okuda M, Miyashiro E, Koike M, Tanaka T, Bouoka M, Okuda S, Yoshikawa N (2002) Serodiagnosis of Helicobacter pylori infection is not accurate for children aged below 10. Pediatr Int 44(4):387–390.  https://doi.org/10.1046/j.1442-200X.2002.01585.x CrossRefGoogle Scholar
  87. Osaki T, Mabe K, Hanawa T, Kamiya S (2008) Urease-positive bacteria in the stomach induce a false-positive reaction in a urea breath test for diagnosis of Helicobacter pylori infection. J Med Microbiol 57(Pt 7):814-819.  https://doi.org/10.1099/jmm.0.47768-0
  88. Osaki T, Okuda M, Ueda J, Konno M, Yonezawa H, Hojo F, Yagyu K, Lin Y, Fukuda Y, Kikuchi S, Kamiya S (2013) Multilocus sequence typing of DNA from faecal specimens for the analysis of intra-familial transmission of Helicobacter pylori. J Med Microbiol 62:761–765.  https://doi.org/10.1099/jmm.0.053140-0
  89. Osaki T, Zaman C, Yonezawa H, Lin Y, Okuda M, Nozaki E, Hojo F, Kurata S, Hanawa T, Kikuchi S, Kamiya S (2018) Influence of intestinal indigenous microbiota on intrafamilial infection by Helicobacter pylori in Japan. Front Immunol 9(287).  https://doi.org/10.3389/fimmu.2018.00287
  90. Ozaydin N, Turkyilmaz SA, Cali S (2013) Prevalence and risk factors of Helicobacter pylori in Turkey: a nationally-representative, cross-sectional, screening with the 13C-Urea breath test. BMC Public Health 13(1215).  https://doi.org/10.1186/1471-2458-13-1215
  91. Papiez D, Konturek PC, Bielanski W, Plonka M, Dobrzanska M, Kaminska A, Szczyrk U, Bochenek A, Wierzchos E (2003) Prevalence of Helicobacter pylori infection in Polish shepherds and their families. Dig Liver Dis 35(1):10–15.  https://doi.org/10.1016/S1590-8658(02)00004-X CrossRefGoogle Scholar
  92. Raj P, Thompson JF, Pan DH (2017) Helicobacter pylori serology testing is a useful diagnostic screening tool for symptomatic inner city children. Acta Paediatr 106(3):470–477.  https://doi.org/10.1111/apa.13724 CrossRefPubMedPubMedCentralGoogle Scholar
  93. Raymond J, Kalach N, Bergeret M, Barbet JP, Benhamou PH, Gendrel D, Dupont C (1996) Evaluation of a serological test for diagnosis of Helicobacter pylori infection in children. Eur J Clin Microbiol Infect Dis 15(5):415–417CrossRefGoogle Scholar
  94. Raymond J, Thiberge JM, Kalach N, Bergeret M, Dupont C, Labigne A, Dauga C (2008) Using macro-arrays to study routes of infection of Helicobacter pylori in three families. PLoS One 3(5):e2259.  https://doi.org/10.1371/journal.pone.0002259 CrossRefPubMedPubMedCentralGoogle Scholar
  95. Rodriguez JM, Murphy K, Stanton C, Ross RP, Kober OI, Juge N, Avershina E, Rudi K, Narbad A, Janmalm MC, Marchesi JR, Collado MC (2015) The composition of the gut microbiota throughout life, with an emphasis on early life. Microb Ecol Health Dis 26(26050).  https://doi.org/10.3402/mehd.v26.26050
  96. Rugge M, Meggio A, Pennelli G, Piscioli F, Giacomelli L, De Pretis G, Graham DY (2007) Gastritis staging in clinical practice: the OLGA staging system. Gut 56(5):631–636.  https://doi.org/10.1136/gut.2006.106666 CrossRefPubMedPubMedCentralGoogle Scholar
  97. Selgrad M, Tammer I, Langner C, Bornschein J, Meißle J, Kandulski A, Varbanova M, Wex T, Schlüter D, Malfertheimer P (2014) Different antibiotic susceptibility between antrum and corpus of the stomach, a possible reason for treatment failure of Helicobacter pylori infection. World J Gastroenterol 20(43):16245–16251. https://doi.org/.  https://doi.org/10.3748/wjg.v20.i43.16245 CrossRefPubMedPubMedCentralGoogle Scholar
  98. Senbanjo IO, Oshikoya KA, Njokanma OF (2014) Helicobacter pylori associated with breastfeeding, nutritional status and recurrent abdominal pain in healthy Nigerian children. J Infect Dev Ctries 8(4):448–453.  https://doi.org/10.3855/jidc.3196
  99. Shady MM, Fathy HA, Ali A, Galal EM, Fathy GA, Sibaii H (2015) Comparison of serum IgG antibody test with gastric biopsy for the detection of Helicobacter pylori infection among Egyptian children. Open Access Maced J Med Sci 3:303–306.  https://doi.org/10.3889/oamjms.2015.062 CrossRefPubMedPubMedCentralGoogle Scholar
  100. Shu X, Ping M, Yin G, Jiang M (2017) Investigation of Helicobacter pylori infection among symptomatic children in Hangzhou from 2007 to 2014: a retrospective study with 12,796 cases. PeerJ 5:e2937.  https://doi.org/10.7717/peerj.2937
  101. Strebel K, Rolle-Kampczyck U, Richter M, Kindler A, Richter T, Schlink U (2010) A rigorous small area modelling-study for the Helicobacter pylori epidemiology. Sci Total Environ 408(18):3931–3942.  https://doi.org/10.1016/j.scitotenv.2010.03.045 CrossRefPubMedPubMedCentralGoogle Scholar
  102. Suerbaum S, Michetti P (2002) Helicobacter pylori infection. N Engl J Med 347(15):1175–1186.  https://doi.org/10.1056/NEJMra020542
  103. Sykora J, Siala K, Varvarovska J, Pazdiora P, Pomahacova 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):286–297.  https://doi.org/10.1111/j.1523-5378.2009.00689.x CrossRefPubMedPubMedCentralGoogle Scholar
  104. Thomas JE, Austin S, Dale A, McClean P, Harding M, Coward WA, Weaver LT (1993) Protection by human milk IgA against Helicobacter pylori infection in infancy. Lancet 342(8863):121.  https://doi.org/10.1016/0140-6736(93)91327-I CrossRefPubMedPubMedCentralGoogle Scholar
  105. Torres J, Perez-Perez G, Goodman KJ, Atherton JC, Gold BD, Harris PR, Ia Garza AM, Guarner J, Munoz O (2000) A comprehensive review of the natural history of Helicobacter pylori infection in children. Arch Med Res 31(5):431–469.  https://doi.org/10.1016/S0188-4409(00)00099-0 CrossRefPubMedPubMedCentralGoogle Scholar
  106. Triantafillidis JK, Gikas A, Hyphantis T, Cheracakis P, Rokkas T, Konstantellou E, Antoniou A, Mallas H, Androulakis G (2002) Helicobacter pylori infection in hospital workers over a 5-year period: correlation with demographic and clinical parameters. J Gastroenterol 37(12):1005–1013.  https://doi.org/10.1007/s005350200170 CrossRefPubMedPubMedCentralGoogle Scholar
  107. Uemura N, Okamoto S, Yamamoto S, Matsumura N, Yamaguchi S, Yamakido M, Taniyama K, Sasaki N, Schiemper RJ (2001) Helicobacter pylori infection and the development of gastric cancer. N Engl J Med 345(11):784–789.  https://doi.org/10.1056/NEJMoa001999 CrossRefPubMedPubMedCentralGoogle Scholar
  108. Urita Y, Watanabe T, Kawagoe N, Takemoto I, Tanaka H, Kijima S, Kido H, Maeda T, Sugasawa Y, Miyazaki T, Honda Y, Nakanishi K, Shimada N, Nakajima H, Sugimoto M, Urita C (2013) Role of infected grandmothers in transmission of Helicobacter pylori to children in a Japanese rural town. J Paediatr Child Health 49(5):394–398.  https://doi.org/10.1111/jpc.12191 CrossRefPubMedPubMedCentralGoogle Scholar
  109. Vandenplas Y, Blecker U, Devreker T, Keppens E, Nijs J, Cadranel S, Pipeleers-Marichal M, Goossens A, Lauwers S (1992) Contribution of the 13C-urea breath test to the detection of Helicobacter pylori gastritis in children. Pediatrics 90(4):608–611PubMedPubMedCentralGoogle Scholar
  110. Westblom TU, Madan E, Gudipati S, Midkiff BR, Czinn SJ (1992) Diagnosis of Helicobacter pylori infection in adult and pediatric patients by using Pyloriset, a rapid latex agglutination test. J Clin Microbiol 30(1):96–98PubMedPubMedCentralGoogle Scholar
  111. Yahaghi E, Khamesipour F, Mashayekhi F, Safarpoor Dehkordi F, Sakhaei MH, Masoudimanesh M, Khameneie MK (2014) Helicobacter pylori in vegetables and salads: genotyping and antimicrobial resistance properties. Biomed Res Int 2014:757941.  https://doi.org/10.1155/2014/757941
  112. Zabala Torres B, Lucero Y, Lagomarcino AJ, Orellana-Manzano A, George S, Torres JP, O’Ryan M (2017) Review: Prevalence and dynamics of Helicobacter pylori infection during childhood. Helicobacter 22(5).  https://doi.org/10.1111/hel.12399
  113. Zamani M, Ebrahimtabar F, Zamani V, Miller WH, Alizadeh-Navaei R, Shokri-Shirvani J, Derakhshan MH (2018) Systematic review with meta-analysis: the worldwide prevalence of Helicobacter pylori infection. Aliment Pharmacol Ther 47(7):868–876.  https://doi.org/10.1111/apt.14561 CrossRefGoogle Scholar
  114. Zhu Y, Zhou X, Wu J, Su J, Zhang G (2014) Risk factors and prevalence of Helicobacter pylori Infection in persistent high incidence area of gastric carcinoma in Yangzhong city. Gastroenterol Res Pract 2014:481365.  https://doi.org/10.1155/2014/481365 PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Kallirroi Kotilea
    • 1
  • Patrick Bontems
    • 1
  • Eliette Touati
    • 2
    Email author
  1. 1.Paediatric Gastroenterology UnitUniversité Libre de Bruxelles, Hôpital Universitaire des Enfants Reine FabiolaBruxellesBelgium
  2. 2.Unit of Helicobacter PathogenesisInstitut PasteurParisFrance

Personalised recommendations