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Research Paper

When is Helicobacter pylori acquired in populations in developing countries? A birth-cohort study in Bangladeshi children

ORCID Icon, ORCID Icon, , , , , & ORCID Icon show all
Pages 252-263 | Received 17 Oct 2017, Accepted 19 Dec 2017, Published online: 01 Mar 2018

References

  • Megraud F, Brassens-Rabbe MP, Denis F, Belbouri A, Hoa DQ. Seroepidemiology of Campylobacter pylori infection in various populations. J Clin Microbiol. 1989;27:1870–3.
  • Torres J, Perez-Perez G, Goodman KJ, Atherton JC, Gold BD, Harris PR, la Garza AM, Guarner J, Munoz O. A comprehensive review of the natural history of Helicobacter pylori infection in children. Arch Med Res. 2000;31:431–69. doi:S0188-4409(00)00099-0
  • Rowland M, Daly L, Vaughan M, Higgins A, Bourke B, Drumm B. Age-specific incidence of Helicobacter pylori. Gastroenterology. 2006;130:65–72; quiz 211. doi:S0016-5085(05)02264-X
  • Miendje Deyi VY, Vanderpas J, Bontems P, Van den Borre C, De Koster E, Cadranel S, Burette A. Marching cohort of Helicobacter pylori infection over two decades (1988-2007): combined effects of secular trend and population migration. Epidemiol Infect. 2011;139:572–80. doi:10.1017/S095026881000110X
  • Perez-Perez GI, Salomaa A, Kosunen TU, Daverman B, Rautelin H, Aromaa A, Knekt P, Blaser MJ. Evidence that cagA(+) Helicobacter pylori strains are disappearing more rapidly than cagA(-) strains. Gut. 2002;50:295–8.
  • den Hoed CM, Vila AJ, Holster IL, Perez-Perez GI, Blaser MJ, de Jongste JC, Kuipers EJ. Helicobacter pylori and the birth cohort effect: evidence for stabilized colonization rates in childhood. Helicobacter. 2011;16:405–9. doi:10.1111/j.1523-5378.2011.00854.x
  • Nakajima S, Nishiyama Y, Yamaoka M, Yasuoka T, Cho E. Changes in the prevalence of Helicobacter pylori infection and gastrointestinal diseases in the past 17 years. J Gastroenterol Hepatol. 2010;25 Suppl 1:S99–S110. doi:10.1111/j.1440-1746.2009.06214.x
  • Chen Y, Blaser MJ. Helicobacter pylori colonization is inversely associated with childhood asthma. J Infect Dis. 2008;198:553–60. doi:10.1086/590158
  • den Hollander WJ, Holster IL, van Gilst B, van Vuuren AJ, Jaddoe VW, Hofman A, Perez-Perez GI, Kuipers EJ, Moll HA, Blaser MJ. Intergenerational reduction in Helicobacter pylori prevalence is similar between different ethnic groups living in a Western city. Gut. 2015;64:1200–8. doi:10.1136/gutjnl-2014-307689
  • Kosunen TU, Aromaa A, Knekt P, Salomaa A, Rautelin H, Lohi P, Heinonen OP. Helicobacter antibodies in 1973 and 1994 in the adult population of Vammala, Finland. Epidemiol Infect 1997;119:29–34.
  • Granstrom M, Tindberg Y, Blennow M. Seroepidemiology of Helicobacter pylori infection in a cohort of children monitored from 6 months to 11 years of age. J Clin Microbiol 1997;35:468–70.
  • Okuda M, Miyashiro E, Booka M, Tsuji T, Nakazawa T. Helicobacter pylori colonization in the first 3 years of life in Japanese children. Helicobacter. 2007;12:324–7. doi:10.1111/j.1523-5378.2007.00510.x
  • O'Ryan ML, Lucero Y, Rabello M, Mamani N, Salinas AM, Pena A, Torres-Torreti JP, Mejias A, Ramilo O, Suarez N, et al. Persistent and transient Helicobacter pylori infections in early childhood. Clin Infect Dis. 2015;61:211–8. doi:10.1093/cid/civ256
  • Mitchell HM, Li YY, Hu PJ, Liu Q, Chen M, Du GG, Wang ZJ, Lee A, Hazell SL. Epidemiology of Helicobacter pylori in southern China: identification of early childhood as the critical period for acquisition. J Infect Dis 1992;166:149–53.
  • Sarker SA, Rahman MM, Mahalanabis D, Bardhan PK, Hildebrand P, Beglinger C, Gyr K. Prevalence of Helicobacter pylori infection in infants and family contacts in a poor Bangladesh community. Dig Dis Sci 1995;40:2669–72.
  • Zabala Torrres B, Lucero Y, Lagomarcino AJ, Orellana-Manzano A, George S, Torres JP, O'Ryan M. Review: Prevalence and dynamics of Helicobacter pylori infection during childhood. Helicobacter. 2012;22:e12399. doi:10.1111/hel.12399.
  • Goodman KJ, Correa P. Transmission of Helicobacter pylori among siblings. Lancet. 2000;355:358–62. doi:S0140-6736(99)05273-3
  • Tindberg Y, Bengtsson C, Granath F, Blennow M, Nyren O, Granstrom M. Helicobacter pylori infection in Swedish school children: lack of evidence of child-to-child transmission outside the family. Gastroenterology. 2001;121:310–6. doi:S0016508501726856
  • Urita Y, Watanabe T, Kawagoe N, Takemoto I, Tanaka H, Kijima S, Kido H, Maeda T, Sugasawa Y, Miyazaki T, et al. Role of infected grandmothers in transmission of Helicobacter pylori to children in a Japanese rural town. J Paediatr Child Health. 2013;49:394–8. doi:10.1111/jpc.12191
  • Perez-Perez GI, Sack RB, Reid R, Santosham M, Croll J, Blaser MJ. Transient and persistent Helicobacter pylori colonization in Native American children. J Clin Microbiol. 2003;41:2401–7.
  • Sarker SA, Mahalanabis D, Hildebrand P, Rahaman MM, Bardhan PK, Fuchs G, Beglinger C, Gyr K. Helicobacter pylori: prevalence, transmission, and serum pepsinogen II concentrations in children of a poor periurban community in Bangladesh. Clin Infect Dis. 1997;25:990–5.
  • Thomas JE, Dale A, Harding M, Coward WA, Cole TJ, Weaver LT. Helicobacter pylori colonization in early life. Pediatr Res. 1999;45:218–23. doi:10.1203/00006450-199902000-00010
  • Ravelomanana L, Imbert P, Kalach N, Ramarovavy G, Richard V, Carod JF, Ravelomanana N, Al Nakib M, Langue J, Avenell C, et al. Helicobacter pylori infection in children in Madagascar: risk factors for acquisition. Trop Gastroenterol. 2013;34:244–51.
  • Rothenbacher D, Inceoglu J, Bode G, Brenner H. Acquisition of Helicobacter pylori infection in a high-risk population occurs within the first 2 years of life. J Pediatr. 2000;136:744–8. doi:S0022-3476(00)77103-4
  • Okuda M, Miyashiro E, Koike M, Okuda S, Minami K, Yoshikawa N. Breast-feeding prevents Helicobacter pylori infection in early childhood. Pediatr Int. 2001;43:714–5. doi:1481
  • Perez-Perez GI, Dworkin BM, Chodos JE, Blaser MJ. Campylobacter pylori antibodies in humans. Ann Intern Med 1988;109:11–7.
  • Morris AJ, Ali MR, Nicholson GI, Perez-Perez GI, Blaser MJ. Long-term follow-up of voluntary ingestion of Helicobacter pylori. Ann Intern Med 1991;114:662–3.
  • Kienesberger S, Cox LM, Livanos A, Zhang XS, Chung J, Perez-Perez GI, Gorkiewicz G, Zechner EL, Blaser MJ. Gastric Helicobacter pylori infection affects local and distant microbial populations and host responses. Cell Rep. 2016;14:1395–407. doi:10.1016/j.celrep.2016.01.017
  • Kienesberger S, Perez-Perez GI, Rivera-Correa JL, Tosado-Acevedo R, Li H, Dubois A, Gonzalez-Martinez JA, Dominguez-Bello MG, Blaser MJ. Serologic host response to Helicobacter pylori and Campylobacter jejuni in socially housed Rhesus macaques (Macaca mulatta). Gut Pathogens. 2012;4:9. doi:10.1186/1757-4749-4-9
  • Zevering Y, Jacob L, Meyer TF. Naturally acquired human immune responses against Helicobacter pylori and implications for vaccine development. Gut 1999;45:465–74.
  • Stenstrom B, Windsor HM, Fulurija A, Benghezal M, Kumarasinghe MP, Kimura K, Tay CY, Viiala CH, Ee HC, Lu W, et al. Helicobacter pylori overcomes natural immunity in repeated infections. Clin Case Rep. 2016;4:1026–33. doi:10.1002/ccr3.687
  • Samloff IM. Cellular localization of group I pepsinogens in human gastric mucosa by immunofluorescence. Gastroenterology 1971;61:185–8.
  • Kim N, Jung HC. The role of serum pepsinogen in the detection of gastric cancer. Gut Liver. 2010;4:307–19. doi:10.5009/gnl.2010.4.3.307
  • Guaraldi F, Salvatori G. Effect of breast and formula feeding on gut microbiota shaping in newborns. Front Cell Infect Microbiol. 2012;2:94. doi:10.3389/fcimb.2012.00094
  • Stordal K, Lundeby KM, Brantsaeter AL, Haugen M, Nakstad B, Lund-Blix NA, Stene LC. Breast-feeding and Infant Hospitalization for Infections: Large Cohort and Sibling Analysis. J Pediatr Gastroenterol Nutr. 2017;65:225–31. doi:10.1097/MPG.0000000000001539
  • Malaty HM, Logan ND, Graham DY, Ramchatesingh JE. Helicobacter pylori infection in preschool and school-aged minority children: effect of socioeconomic indicators and breast-feeding practices. Clin Infect Dis. 2001;32:1387–92. doi:CID000410
  • Thomas JE, Austin S, Dale A, McClean P, Harding M, Coward WA, Weaver LT. Protection by human milk IgA against Helicobacter pylori infection in infancy. Lancet 1993;342:121.
  • Carreira H, Bastos A, Peleteiro B, Lunet N. Breast-feeding and Helicobacter pylori infection: systematic review and meta-analysis. Public Health Nutr. 2015;18:500–20. doi:10.1017/S1368980014000500
  • Perez-Perez GI, Bhat N, Gaensbauer J, Fraser A, Taylor DN, Kuipers EJ, Zhang L, You WC, Blaser MJ. Country-specific constancy by age in cagA+ proportion of Helicobacter pylori infections. Int J Cancer 1997;72:453–6. doi:10.1002/(SICI)1097-0215(19970729)
  • Romero-Gallo J, Perez-Perez GI, Novick RP, Kamath P, Norbu T, Blaser MJ. Responses of endoscopy patients in Ladakh, India, to Helicobacter pylori whole-cell and Cag A antigens. Clin Diagn Lab Immunol. 2002;9:1313–7.
  • Tanriverdi HA, Acun C, Ustundag G, Barut A, Tekin IO, Ustundag Y. Investigation of human colostrum Helicobacter pylori IgA content in lactating women. Eur J Obstet Gynecol Reprod Biol. 2006;124:58–60. doi:S0301-2115(05)00227-7
  • Bhat N, Gaensbauer J, Peek RM, Bloch K, Tham KT, Blaser MJ, Perez-Perez G. Local and systemic immune and inflammatory responses to Helicobacter pylori strains. Clin Diagn Lab Immunol. 2005;12:1393–400. doi:12/12/1393
  • Suerbaum S, Thiberge JM, Kansau I, Ferrero RL, Labigne A. Helicobacter pylori hspA-hspB heat-shock gene cluster: nucleotide sequence, expression, putative function and immunogenicity. Mol Microbiol 1994;14:959–74.
  • Talley NJ, Newell DG, Ormand JE, Carpenter HA, Wilson WR, Zinsmeister AR, Perez-Perez GI, Blaser MJ. Serodiagnosis of Helicobacter pylori: comparison of enzyme-linked immunosorbent assays. J Clin Microbiol 1991;29:1635–9.
  • Eusebi LH, Zagari RM, Bazzoli F. Epidemiology of Helicobacter pylori infection. Helicobacter. 2014;19 Suppl 1:1–5. doi:10.1111/hel.12165
  • Perez-Perez GI, Olivares AZ, Cover TL, Blaser MJ. Characteristics of Helicobacter pylori variants selected for urease deficiency. Infect Immun 1992;60:3658–63.
  • Dunn BE, Roop RM, 2nd, Sung CC, Sharma SA, Perez-Perez GI, Blaser MJ. Identification and purification of a cpn60 heat shock protein homolog from Helicobacter pylori. Infect Immun 1992;60:1946–51. doi:0019-9567/92/051946-06$02.00/0
  • Tummuru MK, Cover TL, Blaser MJ. Cloning and expression of a high-molecular-mass major antigen of Helicobacter pylori: evidence of linkage to cytotoxin production. Infect Immun 1993;61:1799–809.
  • Angelini A, Tosi T, Mas P, Acajjaoui S, Zanotti G, Terradot L, Hart DJ. Expression of Helicobacter pylori CagA domains by library-based construct screening. FEBS J. 2009;276:816–24. doi:10.1111/j.1742-4658.2008.06826.x
  • Koshiol J, Flores R, Lam TK, Taylor PR, Weinstein SJ, Virtamo J, Albanes D, Perez-Perez G, Caporaso NE, Blaser MJ. Helicobacter pylori seropositivity and risk of lung cancer. PLoS One. 2012;7:e32106. doi:10.1371/journal.pone.0032106
  • Ritchie B, Brewster D, Tran CD, McNeil Y, Zacharakis B, Davidson GP, Butler RN. Lack of diagnostic accuracy of the monoclonal stool antigen test for detection of Helicobacter pylori infection in young Australian aboriginal children. Pediatr Infect Dis J. 2009;28:287–9. doi:10.1097/INF.0b013e31818e039b
  • Leal YA, Cedillo-Rivera R, Simon JA, Velazquez 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. doi:10.1097/MPG.0b013e3182077d33
  • Guarner J, Kalach N, Elitsur Y, Koletzko S. Helicobacter pylori diagnostic tests in children: review of the literature from 1999 to 2009. Eur J Pediatr. 2010;169:15–25. doi:10.1007/s00431-009-1033-x
  • Yang HR. Updates on the Diagnosis of Helicobacter pylori Infection in Children: What Are the Differences between Adults and Children? Pediatr Gastroenterol Hepatol Nutr. 2016;19:96–103. doi:10.5223/pghn.2016.19.2.96
  • Seo JH, Park JS, Rhee KH, Youn HS. Limitations of urease test in diagnosis of pediatric Helicobacter pylori infection. World J Clin Pediatr. 2015;4:143–7. doi:10.5409/wjcp.v4.i4.143
  • Malfertheiner P, Schultze V, Rosenkranz B, Kaufmann SH, Ulrichs T, Novicki D, Norelli F, Contorni M, Peppoloni S, Berti D, et al. Safety and immunogenicity of an intramuscular Helicobacter pylori vaccine in noninfected volunteers: a phase I study. Gastroenterology. 2008;135:787–95. doi:10.1053/j.gastro.2008.05.054
  • Okuda M, Miyashiro E, Koike M, Tanaka T, Bouoka M, Okuda S, Yoshikawa N. Serodiagnosis of Helicobacter pylori infection is not accurate for children aged below 10. Pediatr Int. 2002;44:387–90. doi:1585
  • Mittal SK, Mathew JL. Helicobacter pylori infection in children: a review. Trop Gastroenterol. 2003;24:106–15.
  • 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. doi:S0022347604009825
  • 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. doi:S0022-3476(01)11505-2
  • Camorlinga-Ponce M, Torres J, Perez-Perez G, Leal-Herrera Y, Gonzalez-Ortiz B, Madrazo de la Garza A, Gomez A, Munoz O. Validation of a serologic test for the diagnosis of Helicobacter pylori infection and the immune response to urease and CagA in children. Am J Gastroenterol 1998;93:1264–70. doi:S0002-9270(98)00288-3
  • Glassman MS, Dallal S, Berezin SH, Bostwick HE, Newman LJ, Perez-Perez GI, Blaser MJ. Helicobacter pylori-related gastroduodenal disease in children. Diagnostic utility of enzyme-linked immunosorbent assay. Dig Dis Sci 1990;35:993–7.
  • Dubois A, Berg DE, Incecik ET, Fiala N, Heman-Ackah LM, Perez-Perez GI, Blaser MJ. Transient and persistent experimental infection of nonhuman primates with Helicobacter pylori: implications for human disease. Infect Immun 1996;64:2885–91. doi:0019-9567/96/$04.0010
  • Kienesberger S, Perez-Perez GI, Rivera-Correa JL, Tosado-Acevedo R, Li H, Dubois A, Gonzalez-Martinez JA, Dominguez-Bello MG, Blaser MJ. Serologic host response to Helicobacter pylori and Campylobacter jejuni in socially housed Rhesus macaques (Macaca mulatta). Gut Pathog. 2012;4:9. doi:10.1186/1757-4749-4-91757-4749-4-9 [pii]
  • Thomas JE, Bunn JE, Kleanthous H, Monath TP, Harding M, Coward WA, Weaver LT. Specific immunoglobulin A antibodies in maternal milk and delayed Helicobacter pylori colonization in Gambian infants. Clin Infect Dis. 2004;39:1155–60. doi:10.1086/424514
  • Bunn JE, Thomas JE, Harding M, Coward WA, Weaver LT. Placental acquisition of maternal specific IgG and Helicobacter pylori colonization in infancy. Helicobacter. 2003;8:568–72. doi:10.1046/j.1523-5378.2003.00178.x
  • Bhuiyan TR, Saha A, Lundgren A, Qadri F, Svennerholm AM. Immune responses to Helicobacter pylori infection in Bangladeshi children during their first two years of life and the association between maternal antibodies and onset of infection. J Infect Dis. 2010;202:1676–84. doi:10.1086/657085
  • Rothenbacher D, Winkler M, Gonser T, Adler G, Brenner H. Role of infected parents in transmission of Helicobacter pylori to their children. Pediatr Infect Dis J. 2002;21:674–9. doi:10.1097/01.inf.0000021081.69738.42
  • Nahar S, Kibria KM, Hossain ME, Sultana J, Sarker SA, Engstrand L, Bardhan PK, Rahman M, Endtz HP. Evidence of intra-familial transmission of Helicobacter pylori by PCR-based RAPD fingerprinting in Bangladesh. Eur J Clin Microbiol Infect Dis. 2009;28:767–73. doi:10.1007/s10096-008-0699-8
  • Kennemann L, Didelot X, Aebischer T, Kuhn S, Drescher B, Droege M, Reinhardt R, Correa P, Meyer TF, Josenhans C, et al. Helicobacter pylori genome evolution during human infection. Proc Natl Acad Sci U S A. 2011;108:5033–8. doi:10.1073/pnas.1018444108
  • Schwarz S, Morelli G, Kusecek B, Manica A, Balloux F, Owen RJ, Graham DY, van der Merwe S, Achtman M, Suerbaum S. Horizontal versus familial transmission of Helicobacter pylori. PLoS Pathog. 2008;4:e1000180. doi:10.1371/journal.ppat.1000180
  • Marshall BJ, Armstrong JA, McGechie DB, Glancy RJ. Attempt to fulfil Koch's postulates for pyloric Campylobacter. Med J Aust 1985;142:436–9.
  • Graham DY, Opekun AR, Osato MS, El-Zimaity HM, Lee CK, Yamaoka Y, Qureshi WA, Cadoz M, Monath TP. Challenge model for Helicobacter pylori infection in human volunteers. Gut. 2004;53:1235–43. doi:10.1136/gut.2003.037499
  • Stromqvist M, Falk P, Bergstrom S, Hansson L, Lonnerdal B, Normark S, Hernell O. Human milk kappa-casein and inhibition of Helicobacter pylori adhesion to human gastric mucosa. J Pediatr Gastroenterol Nutr. 1995;21:288–96.
  • Sakamoto I, Igarashi M, Kimura K, Takagi A, Miwa T, Koga Y. Suppressive effect of Lactobacillus gasseri OLL 2716 (LG21) on Helicobacter pylori infection in humans. J Antimicrob Chemother. 2001;47:709–10.
  • Ryan KA, Daly P, Li Y, Hooton C, O'Toole PW. Strain-specific inhibition of Helicobacter pylori by Lactobacillus salivarius and other lactobacilli. J Antimicrob Chemother. 2008;61:831–4. doi:10.1093/jac/dkn040
  • de Klerk N, Maudsdotter L, Gebreegziabher H, Saroj SD, Eriksson B, Eriksson OS, Roos S, Linden S, Sjolinder H, Jonsson AB. Lactobacilli reduce Helicobacter pylori attachment to host gastric epithelial cells by inhibiting adhesion gene expression. Infect Immun. 2016;84:1526–35. doi:10.1128/IAI.00163-16
  • Arnold IC, Lee JY, Amieva MR, Roers A, Flavell RA, Sparwasser T, Muller A. Tolerance rather than immunity protects from Helicobacter pylori-induced gastric preneoplasia. Gastroenterology. 2011;140:199–209. doi:10.1053/j.gastro.2010.06.047
  • Sinha SK, Martin B, Gold BD, Song Q, Sargent M, Bernstein CN. The incidence of Helicobacter pylori acquisition in children of a Canadian First Nations community and the potential for parent-to-child transmission. Helicobacter. 2004;9:59–68.
  • Biswas M, Roy DN, Tajmim A, Rajib SS, Hossain M, Farzana F, Yasmen N. Prescription antibiotics for outpatients in Bangladesh: a cross-sectional health survey conducted in three cities. Ann Clin Microbiol Antimicrob. 2014;13:15. doi:10.1186/1476-0711-13-15
  • Hasan K, Jolly P, Marquis G, Roy E, Podder G, Alam K, Huq F, Sack R. Viral etiology of pneumonia in a cohort of newborns till 24 months of age in Rural Mirzapur, Bangladesh. Scand J Infect Dis. 2006;38:690–5. doi:N04747837306445P
  • Pathela P, Hasan KZ, Roy E, Alam K, Huq F, Siddique AK, Sack RB. Enterotoxigenic Bacteroides fragilis-associated diarrhea in children 0–2 years of age in rural Bangladesh. J Infect Dis. 2005;191:1245–52. doi:10.1086/428947
  • Blaser MJ, Perez-Perez GI, Kleanthous H, Cover TL, Peek RM, Chyou PH, Stemmermann GN, Nomura A. Infection with Helicobacter pylori strains possessing cagA is associated with an increased risk of developing adenocarcinoma of the stomach. Cancer Res 1995;55:2111–5.
  • Hook-Nikanne J, Perez-Perez GI, Blaser MJ. Antigenic characterization of Helicobacter pylori strains from different parts of the world. Clin Diagn Lab Immunol 1997;4:592–7.
  • Filteau SM, Rice AL, Ball JJ, Chakraborty J, Stoltzfus R, de Francisco A, Willumsen JF. Breast milk immune factors in Bangladeshi women supplemented postpartum with retinol or beta-carotene. Am J Clin Nutr. 1999;69:953–8.

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