Review articles

By Dr. Sukhbir Shahid
Corresponding Author Dr. Sukhbir Shahid
Pediatrics, - India
Submitting Author Dr. Sukhbir Shahid

H.pylori, Gastritis, Children, Peptic ulcer disease

Shahid S. Helicobacter Pylori Infection in Children. WebmedCentral PAEDIATRICS 2012;3(8):WMC003664
doi: 10.9754/journal.wmc.2012.003664

This is an open-access article distributed under the terms of the Creative Commons Attribution License(CC-BY), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Submitted on: 23 Aug 2012 04:41:46 PM GMT
Published on: 24 Aug 2012 02:32:56 PM GMT


H.pylori is a widely prevalent and important component of gastric microbiology. It is usually acquired in childhood. It is more common in poorer sections of society especially of developing countries. It can cause peptic ulcer disease and dyspepsia. It is a potent carcinogen responsible for gastric adenocarcinoma and gastric lymphoma. H.pylori infection should be suspected in children with history suggestive of hyperacidity and in those who have a first degree family member with gastric cancer. Diagnosis relies on endoscopy and biopsy. Non-invasive tests on breath, stool, serum, urine and saliva can also diagnose H.pylori infection reliably. Treatment in children involves a triple regimen comprising of proton pump inhibitor or bismuth compounds with either two antibiotics or one antibiotic and an imidazole. This eradicates the organism in >90% of the patients. The above tests may need to be repeated to confirm on clearance of the bacterial infection. Awareness of H.pylori infection is vital due to its high rate of colonization and risk of gastric malignancies.


Helicobacter pylori (H. pylori) is an important pathogen of paediatric gastroenterology [1, 2]. They are acquired in early childhood [3-7], and are more common in socially deprived people of the developing countries [2, 8, 9]. More than half of the world’s population is infected with this bacteria [10, 11]. Infection rates are similar in both sexes, though some studies have noted a slight male predominance [2]. Prevalence increases with age and it is more common in Asians and Africans [2, 11-13]. The clinical implication of this infection in children is still in the evolution phase. H.pylori infection in children differs from that in adults in its prevalence, presence, site and degree of gastric/duodenal inflammation, lesser likelihood of gastric malignancies, problems in diagnosis and higher rate of antibiotic resistance [14].


H.pylori is a gram-negative helical microaerophilic flagellated bacterium found in the sterile gastric mucosa of majority of the world’s population [15]. Bacterial presence in stomach was known as early as in the late 19th century. However these were dispelled as contaminants from digested foods rather than true colonizers [10, 16]. It was only 3 decades back that there was renewed interest in the microbiology of the stomach with the discovery and successful isolation and culture of the H. pylori (formerly called Campylobacter pylori) [17-19]. Further research showed that these organisms caused a variety of gastrointestinal disorders such as chronic/atrophic gastritis, peptic ulcer disease, gastric non-Hodgkin’s lymphoma and gastric adenocarcinoma [10].


Helicobacter pylori prevalence varies depending on the geographic region, age, race, ethnicity and socio-economic status of individual. Helicobacter pylori reside in more than 80% of the stomach of people in the developing world and 40% of those in the western world. High prevalence has been found in general population from Bangladesh, Brazil, Russia, Mexico and Korea. It has also been noted to be high in institutionalized adults from UK and other countries [20-26]. The lowest reported has been in Czech Republic at 7.1% in children < 15 years of age [27]. Decline in prevalence has been noted in the Western figures. The number of people colonized is inversely proportional to the socioeconomic status, and increases with age [28, 29].

Microbiological characteristics

H.pylori belongs to the genus Helicobacter, family Helicobacteraceae, order Campylobacterales, and ? subdivision of Proteobacteria. It is an S-shaped gram-negative rod measuring 2-5 ?m in length and 0.5-1 ?m in width. It has 1-3 turns but acquires rod or coccoid shape with prolonged in vitro culture or after antibiotic therapy [30-32]. The coccoid forms are considered as dead cells, but some believe that they are viable but nonculturable bacilli [33]. This helical organism is motile by means of 2-6 sheathed unipolar flagellae; about 3 ?m long with a bulb at the end [34]. Unlike most enteric bacteria, H. pylori lacks fimbrial adhesions.  Its cell envelope consists of an outer and inner plasma membranes separated by a 30 nm thick periplasm. The dense cytoplasm contains nucleoid material, ribosomes and intracellular polyphosphate granules [35, 36]. Cytoplasmic aggregates containing iron are present in these bacteria and they represent tools for survival during inhospitable circumstances [37].

H.pylori requires low oxygen concentrations of 2-5%, 5-10% CO2, high humidity, 370C temperature and neutral pH for optimal growth. It is fastidious requiring complex blood or serum supplemented growth media [10]. Columbia or brucella agar supplemented with lysed horse or sheep blood or fetal or newborn calf serum is routinely used solid media for culture and isolation. Brucella, Mueller-Hinton or brain heart infusion broth enriched with 2-10% calf serum or 0.2-1.0% ?-cyclodextrins are the liquid growth media recommended. 98-100% humid conditions are provided to the media. The specimen needs to be cultured for atleast 14 days and H.pylori forms small, smooth, translucent colonies [38]. It is urease, catalase, and oxidase positive. H.pylori can metabolize glucose but not other sugars [10, 39-41]. Due to the enzyme urease, it can degrade urea forming ammonia and bicarbonate which facilitates its survival and growth in the acidic gastric environment. These neutralise the gastric pH and are cytotoxic for the gastric cells. H.plori can withstand short periods of exposure to pH < 4 [42, 43]. Its motility and abundance of urease enzyme assists its penetration into the gastric mucus layer.

Transmission and pathogenesis

The exact route of transmission of H.pylori remains elusive. But it is believed to spread via direct human-to-human transmission through oral-oral, feco-oral or both routes. H.pylori is present in saliva, vomitus, gastric reflux material and stools of infected individuals and non-human primates [44-47]. Overcrowding is a risk factor for acquisition of H.pylori infection in children [48, 49]. Contaminated water and food also act as sources of infection [50, 51]. But since H.pylori cannot withstand high oxygen, high temperatures and paucity of nutrients in the environment, it does not remain viable in inhospitable conditions. Hence direct person-to-person transmission is thought to be still the main mode of transmission of this infection in children [10].

Colonization by H.pylori does not imply disease but its presence increases lifetime risk of the child getting peptic ulcer disease or gastric cancer by 10-20% and 1-2% respectively [52-55]. This risk is dependent on a complex interplay between bacterial, host and environmental factors. H.pylori is able to withstand the hostile acidic milieu of the stomach due to its urease-secreting capacity. Their spiral structure and flagellae assist in their movements into the neutral gastric mucus layer. Here they induce an inflammatory process of Th1 type; involving neutrophiles, mononuclear cells, and T-helper 1 cells [56]. They initially cause acute gastritis and hypochlorhydria, followed by chronic gastritis and/or atrophic gastritis [57, 58]. The infection may resolve [59] or progress to peptic ulcer disease. Studies carried out in the developed world have shown that eradication of H.pylori reduces risk of recurrence in peptic ulcer disease [10, 60]. With increasing time, there is loss of normal gastric mucosa architecture, destruction of gastric glands, epithelial cell damage, fibrosis, DNA damage, mutations, and intestinal metaplasia and dysplasia [61]. These effects could lead to gastric adenocarcinoma [62-64]. Risk of gastric cancer is elevated 10 times and hence H.pylori has been labelled as a class I carcinogen by World Health Organization [65]. When one clone of B cells proliferates, gastric lymphoma ensues [10, 66].

Clinical features

H.pylori is usually acquired during early childhood [67]. It may be asymptomatic. Even in cases with histologically proven chronic gastritis, symptoms may be lacking [10]. In some, it gives rise to symptoms of peptic ulcer disease or its complications [54]. There may be non-ulcer dyspepsia, or refractory iron-deficiency anemia [68-70]. In long-standing cases, gastric cancer or lymphoma may be seen [62, 66]. The symptoms result due to the complex, less understood interaction between the bacterial, host and environmental factors. Child’s stature and weight is usually not affected due to H.pylori colonization but there may be anorexia and weight loss due to peptic-ulcer disease [71]. A number of extragastroduodenal disorders such as coronary artery disease, idiopathic urticaria, rosacea, scleroderma, otitis media, upper airway infections, periodontal disease, food allergy, sudden infant death syndrome, idiopathic thrombocytopenia, short stature, autoimmune diseases, Raynaud’s phenomenon, migraine, and Guillian-Barre syndrome have been thought to be due to H.pylori infection [10, 72, 73]. Various mechanisms have been postulated for this association. But more randomized studies are needed to confirm the role of H.pylori in these disorders [14, 74-76]. However in case of idiopathic thrombocytopenic purpura, the association is more or less confirmed in adults due to the fact that eradication of H.pylori was found to improve thrombocyte counts [77-79]. However in children this cause-effect relationship has yet not been proven. Recent studies in mice have shown that H.pylori infection can protect against asthma. Overuse of antibiotics has abolished this ancestral, native microflora leading to immune upset and asthma [80].


A multitude of tests can be used to diagnose presence of H.pylori in the stomach. Invasive endoscopy and thence culture, histopathology, rapid urease test, polymerase chain reaction (PCR) or fluorescence in-situ hybridization (FISH) is feasible in children and is considered the gold standard for diagnosis of H.pylori infection [81-85]. Culture of the bacteria from biopsied gastric tissue has 100% specificity but its sensitivity is lower. 2 of 3 of the above tests performed should be negative to rule out H.pylori infection. Urea breath test is the alternative non-invasive gold standard for diagnosis of H.pylori. It is safe, reliable and useful with specificity and sensitivity of >95%. However, it needs patient cooperation hence it is not possible in infants, toddlers, and in some children with special needs. Instrument required is also expensive. In this, patient is made to swallow urea labelled with isotope C13 or C14. Urea is broken down by urease of H.pylori, CO2 is released and excreted through the breath. Measurement of labelled CO2 before and 20-30 minutes after urea ingestion is performed. The difference gives an indication about presence of gastric H.pylori [86]. The above two tests could also be used to evaluate success of eradication of H.pylori after treatment. Fecal antigen test detects H.pylori antigen in stool of patient [87]. It is also a simple, non-invasive and reliable test. It however cannot be used to confirm success of eradication therapy. Serological testing for antibodies to H.pylori has lower specificity and sensitivity and cannot be used for routine screening. It is mainly used for epidemiological surveys. It cannot however be relied on for estimation of success of anti-H.pylori therapy due to immunological memory. Saliva could be used for measurement of immunoglobulin G against H.pylori non-invasively and this has been found to be quite reliable [88-93]. These tests are indicated in children with history suggestive of peptic ulcer disease, those with first-degree relatives with gastric cancer, and in children with refractory iron-deficiency anaemia where other causes have been ruled out. They are not indicated in children with functional abdominal pain or idiopathic thrombocytopenia [94, 95].


H.pylori is susceptible to a number of antibiotics in vitro but in vivo these fail as monotherapy due to bacterial resistance. Resistance is mainly due to point mutations on the bacterial chromosomes (nonsense, missense, and silent mutations). These may involve various genes such as redox-related genes or 23S rRNA [96]. Clarithromycin can eradicate this infection in 40% of users when taken two times a day for 10-14 days [97, 98]. For better clearance, ‘concomitant’ (standard triple or quadruple) or ‘sequential’ therapies are preferred. This implies combining 2-3 antibiotics with either proton pump inhibitor [PPI] or bismuth salts. Combining PPI with dual antibiotics improves eradication rate from 9.4% to 74.2% [99]. This triple regime is considered as first line therapy in pediatric guidelines for H.pylori [94, 100, 101]. PPI+amoxicillin+imidazole or PPI+amoxicillin+clarithromycin or bismuth salts+amoxicillin+imidazole is recommended. In sequential therapy, PPI+amoxicillin for 5 days followed by PPI+clarithromycin+imidazole for 5 days are used. However, falling clearance rates have been reported with this recommended treatment either due to non-compliance due to adverse effects and/or due to antibiotic resistance [102, 103]. In such cases, susceptibility testing guided therapy is effective and cures >90% of children treated [104-108]. Therapies may need to be individualized based on age, other demographic parameters and host polymorphisms. Use of probiotic, Saccharomyces Boulardii could serve as a useful adjunct to antibiotic therapy [109, 110]

PPI decreases gastric acidity and it aids in bacterial eradication. Mechanism of action of bismuth is unknown but in vivo and in vitro studies have proven it to be effective in eliminating H.pylori [111-113]. It is supposed to lyse cell walls, prevent adherence of bacteria to epithelium and inhibit urease enzyme. The antibiotics and imidazole drugs used are bactericidal. Amoxycillin, macrolides [clarithromycin or azithromycin], imidazoles [metronidazole or tinidazole], or tetracycline are employed [114]. Rifabutin and furazolidine are used as second-line drugs in metronidazole-resistant cases [115-119]. Fluoroquinolones such as ciprofloxacin and levofloxacin, rifampin, streptomycin can be used but offer no advantages over the recommended first-line antibacterial agents [120-122]. Some studies have shown that bismuth-based therapies are more effective and less costly than PPI-based therapies [102]. However, unpleasant taste and unpalatability of bismuth raises concern about the compliance of bismuth-based therapies and hence its ultimate clearance rates. Longer duration of therapy enhances eradication rates in children [123] (Table 1).

see Illustration 1

A non-invasive test to confirm eradication of H.pylori should be done after 4-8 weeks of treatment. In case of failure of therapy, use of different antibiotics, adding bismuth, increasing dose and/or duration helps. Endoscopy and susceptibility studies may be needed to guide therapy.

Besides proper treatment, vaccination could control this infection. Trials on vaccines for prevention are ongoing and have shown promising results. Suitable immunogens, adjuvants and route of immunization could improve outcomes [124-127]. If human trials are successful, it could have important health-related implications.


H.pylori colonization is common in pediatric age group. Symptoms due to this though uncommon do occur, and would need proper diagnosis and treatment. The goal of therapy is to eradicate the organism in the first attempt and avoid development of resistance. Adherence to prescribed therapy should be ensured. This would greatly aid in minimising later risk of dysplasia and gastric cancer and gastric lymphoma.


1. Perez-Perez GI, Taylor DN, Bodhidatta L et al Seroprevalence of Helicobacter pylori infections in Thailand J Infect Dis 1990; 161: 1237-1241
2. Ndip RN, Malange AE, Akoachere JF, MacKay WG, Titanji VP, Weaver LT. Helicobacter pylori antigens in the faeces of asymptomatic children in the Buea and Limbe health districts of Cameroon: a pilot study. Trop Med Int Health 2004; 9[9]: 1036-1040
3. Banatvala N, Mayo K, Megraud F et al The cohort effect and Helicobacter pylori J Infect Dis 1993; 168: 219-221
4. O’Donohoe JM, Sullivan PB, Scott R et al Recurrent abdominal pain and Helicobacter pylori in a community-based sample of London children. Acta Pediatr 1996; 85: 961-964
5. Lindkvist P, Asrat D, Nilsson I et al Age at acquisition of Helicobacter pylori infection: comparison of a high and low prevalence country. Scand J Infect Dis 1996; 28:181-184
6. Mitchell HM, Li YY, Hu PJ et al Epidemiology of Helicobacter pylori in Southern China: identification of early childhood as the critical period for acquisition. J Infect Dis 1992; 166:149-153
7. Rowland M, Imrie C, Bourke B, Drumm D. How should Helicobacter pylori infected children be managed? Gut 1999; 45: 136-139
8. Kusters JG, van Vliet AHM, Kuipers EJ. Pathogenesis of Helicobacter Pylori infection Clinical Microbiology Reviews 2006; 19: 449-490
9. Fiedorek SC, Malaty HM, Evans DM, Pumphrey CL, Casteel HB, Evans Jr. DJ, Graham DY Factors influencing the epidemiology of Helicobacter Pylori infection in children Pediatrics 1991; 88: 578-582
10. Ernst PB, Gold BD. Helicobacter pylori in childhood: new insights into the immunopathogenesis of gastric disease and implications for managing infection in children. J Pediatr Gastroenterol Nutr.1999; 28: 462-473
11. Gold BD, Colletti RB, Abbot M, Czinn SJ, Elitsur Y, Hassal E, Macarthur C, Synder J, Sherman PM. Helicobacter pylori Infection in Children: Recommendations for Diagnosis and Treatment. Journal of Pediatric Gastroenterology and Nutrition 2000; 31: 490-497
12. Sullivan PB, Thomas JE, Wight DG et al. Helicobacter pylori in Gambian children with chronic diarrhoea and malnutrition. Arch Dis Child 1990; 65[2]: 189-191
13. Koletzko S, Richy F, Bontems P, Crone J, Kalach N, Monteiro L, et al. Prospective multicenter study on antibiotic resistance of Helicbacter pylori strains obtained from children living in Europe. Gut 2006; 55[12]: 1711-1716
14. Koletzko S, Jones NL, Goodman KJ, Gold B, Rowland M, Cadranel S, Chong S, Colletti RB, Casswall T, Elitsur Y, Guarner J, Kalach N, Madrazo A,  Megraud F, Oderda G on behalf of the H. pylori working groups of ESPGHAN and NASPGHAN. Evidence-based guidelines from ESPGHAN and NASPGHAN for Helicobacter pylori infection in children Journal of Pediatric Gastroenterology and Nutrition 2011; 53: 230-243
15. Blecker U Helicobacter pylori-associated gastroduodenal disease in childhood. South Med J 1997; 90[6]: 570-576
16. Bizzozero G Ueber die schlauchfo¨rmigen Dru¨sen des Magendarmkanals und die Beziehungen ihres Epithels zu dem Oberfla¨chenepithel der Schleimhaut Dritte mitteilung Archiv Mikroskopische Anat 1893; 43: 82-152
17. Marshall BJ, Armstrong JA, McGechie DB, Glancy RJ Attempt to fulfil Koch’s postulates for pyloric Campylobacter Med J Austr 1985; 142: 436-439
18. Morris A, Nicholson G Ingestion of Campylobacter pyloridis causes gastritis and raised fasting gastric pH. Am J Gastroenterol 1987; 82: 192-199
19. 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: 662–663
20. Ahmad MM, Rahman M, Rumi AK et al. Prevalence of Helicobacter pylori in asymptomatic population-a pilot serological study in Bangladesh. J Epidemiol 1997; 7: 251-254
21. Souto FJ, Fontes CJ, Rocha GA et al. Prevalence of Helicobacter pylori infection in a rural area of the state of Matto Grasso, Brazil. Mem Inst Oswaldo Cruz 1998; 93: 171-174
22. Malaty HM, Paykov V, Bykova O et al. Helicobacter pylori and socioeconomic factors in Russia. Helicobacter 1996; 1: 82-87
23. Torres J, Leal Herrera Y, Perez-Perez G et al. A community-based seroepidemiologic study of Helicobacter pylori infection in Mexico J Infect Dis 1998; 178: 1089-1094
24. Malaty HM, Kim JG, Kim SD et al. Prevalence of Helicobacter pylori infection in Korean children; inverse relation to socioeconomic status despite a uniformly high prevalence in adults. Am J Epidemiol 1996; 143: 257-262
25. Harris AW, Douds A, Meurisse EV et al. Seroprevalence of Helicobacter pylori in residents of a hospital for people with severe learning difficulties. Eur J Gastroenterol Hepatol 1995; 7: 21-23
26. Lambert JR, Lin SK, Sievert W et al. High prevalence of Helicobacter pylori antibodies in an institutionalized population: evidence for person-to-person transmission. Am J Gastroenterol 1995; 90: 2167-2171
27. Sýkora J, Siala K, Varvarovská J, Pazdiora P, Pomahacová R, Huml M 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 2009;14(4): 286-297
28. Perez-Perez GI, Rothenbacher D, Brenner H Epidemiology of Helicobacter pylori infection Helicobacter 2004; 9 [Suppl 1]: 1-6
29. Pounder RE, Ng D The prevalence of Helicobacter pylori infection in different countries. Aliment. Pharmacol. Ther 1995; 9: 33-39
30. Kusters JG, Gerrits MM, van Strijp JA, Vandenbroucke- Grauls CM. Coccoid forms of Helicobacter pylori are the morphologic manifestation of cell death. Infect. Immun 1997; 65: 3672-3679
31. Goodwin CS, McCulloch RK, Armstrong JA, Wee SH. Unusual cellular fatty acids and distinctive ultrastructure in a new spiral bacterium (Campylobacter pyloridis) from the human gastric mucosa J Med Microbiol 1985; 19: 257-267
32. Jones DM, Curry A, Fox AJ An ultrastructural study of the gastric campylobacter-like organism Campylobacter pyloridis  J Gen Microbiol 1985; 131: 2335-2341
33. Enroth H, Wreiber K, Rigo R, Risberg D, Uribe A, Engstrand L. In vitro aging of Helicobacter pylori: changes in morphology, intracellular composition and surface properties. Helicobacter 1999; 4: 7-16
34. O’Toole PW, Lane MC, Porwollik S. Helicobacter pylori motility. Microbes Infect 2000;  2: 1207-1214
35. Costa K, Bacher G, Allmaier G, Dominguez-Bello MG, Engstrand L, Falk P, de Pedro MA, Garcia-del Portillo F The morphological transition of Helicobacter pylori cells from spiral to coccoid is preceded by a substantial modification of the cell wall. Microbiology 1999; 181: 3710-3715
36. Bode G, Mauch F, Ditschuneit H, Malfertheiner P Identification of structures containing polyphosphate in Helicobacter pylori J Gen Microbiol 1993; 139: 3029-3033
37. Bereswill S, Waidner U, Odenbreit S, Lichte F, Fassbinder F, Bode G, Kist M Structural, functional and mutational analysis of the pfr gene encoding a ferritin from Helicobacter pylori  Microbiology 1998; 144: 2505-2516
38. Han SW, Flamm R, Hachem CY, Kim HY, Clarridge JE, Evans DG, Beyer J, Drnec J, Graham DY Transport and storage of Helicobacter pylori from gastric mucosal biopsies and clinical isolates Eur J Clin Microbiol Infect Dis 1995; 14: 349-352
39. Marcus EA, Scott DR Cell lysis is responsible for the appearance of extracellular urease in Helicobacter pylori Helicobacter 2001; 6: 93-99
40. Marais A, Mendz GL, Hazell SL, Megraud F Metabolism and genetics of Helicobacter pylori: the genome era Microbiol Mol Biol Rev 1999; 63: 642-674
41. Nedenskov P Nutritional requirements for growth of Helicobacter pylori Appl Environ Microbiol 1994; 60: 3450-3453
42. Scott DR, Marcus EA, Weeks DL, Sachs G Mechanisms of acid resistance due to the urease system of Helicobacter pylori Gastroenterology 2002; 123: 187-195
43. Stingl K, Altendorf K, Bakker EP. Acid survival of Helicobacter pylori: how does urease activity trigger cytoplasmic pH homeostasis? Trends Microbiol 2002; 10:70-74
44. Allaker RP, Young KA, Hardie JM, Domizio P, Meadows NJ Prevalence of Helicobacter pylori at oral and gastrointestinal sites in children: evidence for possible oral-to-oral transmission J Med Microbiol 2002; 51: 312-317
45. Ferguson DA Jr., Li C,  Patel NR, Mayberry WR, Chi DS, Thomas E Isolation of Helicobacter pylori from saliva J Clin Microbiol 1993; 31: 2802-2804
46. Kabir S. Detection of Helicobacter pylori DNA in feces and saliva by polymerase chain reaction: a review. Helicobacter 2004; 9: 115-123
47. Leung WK, Siu KL, Kwok CK, Chan SY, Sung R, Sung JJ Isolation of Helicobacter pylori from vomitus in children and its implication in gastro-oral transmission Am J Gastroenterol 1999; 94: 2881-2884
48. Goodman KJ, Correa P. Transmission of Helicobacter pylori among siblings. Lancet 2000; 355: 358-362
49. Raymond J, Thiberg JM, Chevalier C, Kalach N, Bergeret M, Labigne A, Dauga C Genetic and transmission analysis of Helicobacter pylori strains within a family Emerg Infect Dis 2004; 10: 1816-1821
50. Lu Y, Redlinger TE, Avitia R, Galindo A, Goodman K Isolation and genotyping of Helicobacter pylori from untreated municipal wastewater Appl Environ Microbiol 2002;  68: 1436-1439
51. Poms RE, Tatini SR Survival of Helicobacter pylori in ready-to-eat foods at 4 degrees C Int J Food Microbiol 2001; 63: 281-286
52. Ernst PB, Gold BD The disease spectrum of Helicobacter pylori: the immunopathogenesis of gastroduodenal ulcer and gastric cancer. Annu Rev Microbiol 2000; 54: 615-640
53. Kuipers EJ Review article: exploring the link between Helicobacter pylori and gastric cancer Aliment Pharmacol Ther 1999; 13: 3-12
54. Kuipers EJ, Thijs JC, Festen HP The prevalence of Helicobacter pylori in peptic ulcer disease  Aliment Pharmacol Ther 1995; 9[Suppl. 2]: 59-69
55. Sipponen P, Varis K, Fra¨ki O, Korri UM, Seppa¨la¨ K, Siurala M Cumulative 10-year risk of symptomatic duodenal and gastric ulcer in patients with or without chronic gastritis Scand J Gastroenterol 1990; 25: 966-973
56. Correa P, Haenszel W, Cuello C, Tannenbaum S, Archer M A model for gastric cancer epidemiology Lancet 1975; 2: 58-59
57. Morris A, Nicholson G Ingestion of Campylobacter pyloridis causes gastritis and raised fasting gastric pH Am J Gastroenterol 1987; 82: 192-199
58. Graham DY, Alpert LC, Smith JL, Yoshimura HH Iatrogenic  Campylobacter pylori infection is a cause of epidemic achlorhydria Am J Gastroenterol 1988;  83: 974-980
59. Malaty HM, Graham DY, Wattigney WA, Srinivasan SR, Osato M, Berenson GS Natural history of Helicobacter pylori infection in childhood: 12-year follow-up cohort study in a biracial community Clin Infect Dis 1999;  28: 279-282
60. Rauws EAJ, Tytgat GNJ  Cure of duodenal ulcer associated with eradication of Helicobacter pylori Lancet 1990; 335: 1233-1235
61. Kuipers EJ, Uyterlinde AM, Pena AS, Roosendaal R, Pals G, Nelis GF, Festen HP, Meuwissen SG Long-term sequelae of Helicobacter pylori gastritis Lancet 1995; 345: 1525-1528
62. Sipponen P, Kekki M, Haapakoski J, Ihamaki T, Siurala M Gastric cancer risk in chronic atrophic gastritis: statistical calculations of cross-sectional data Int J Cancer 1985; 35: 173-177
63. Forman D, Sitas F, Newell DG, Stacey AR, Boreham J, Peto R, Campbell TC, Li J, Chen J Geographic association of Helicobacter pylori antibody prevalence and gastric cancer mortality in rural China Int J Cancer 1990; 46:608-611
64. The Eurogast Study Group An international association between Helicobacter pylori infection and gastric cancer Lancet 1993; 341: 1359-1362
65. International Agency for Research on Cancer IARC monographs on the evaluation of carcinogenic risks to humans, vol. 61: schistosomes, liver flukes and Helicobacter pylori. 1994 International Agency for Research on Cancer, Lyon, France
66. Parsonnet J, Hansen S, Rodriguez L, Gelb AB, Warnke RA, Jellum E, Orentreich N,  Vogelman JH, Friedman GD Helicobacter pylori infection and gastric lymphoma N Engl J Med 1994; 330: 1267-1271
67. Allaker RP, Young KA, Hardie JM, Domizio P, Meadows NJ Prevalence of Helicobacter pylori at oral and gastrointestinal sites in children: evidence for possible oral-to-oral transmission J Med Microbiol 2002; 51: 312-317
68. Talley NJ, Hunt RH What role does Helicobacter pylori play in dyspepsia and nonulcer dyspepsia? Arguments for and against H. pylori being associated with dyspeptic symptoms. Gastroenterology 1997; 113: S67–S77
69. Qu XH, Huang XL, Xiong P et al. Does Helicobacter pylori infection play a role in iron deficiency anemia? A meta-analysis World J Gastroenterol 2010; 16: 886–896
70. Cardenas VM,  Prieto-Jimenez CA, Mulla ZD, Rivera JO, Dominguez DC, Graham DY, Ortiz M Helicobacter pylori eradication and change in markers of iron stores among non–iron-deficient children in El Paso, Texas: An etiologic intervention study Journal of Pediatric Gastroenterology & Nutrition 2011; 52: 326-332
71. Sood MR, Joshi S, Akobeng A, Mitchell J, Thomas AG Growth in children with Helicobacter pylori infection and dyspepsia ADC 2005; 90: 1025-1028
72. Gasbarrini A, Carloni E, Gasbarrini G, Chisholm SA Helicobacter pylori and extragastric diseases-other Helicobacters Helicobacter 2004; 9[Suppl 1]: 57–66
73. Hasni S, Ippolito A, Illei GG. Helicobacter pylori and autoimmune diseases Oral diseases 2011; 17: 621-627
74. Bamford JTM, Tilden RL, Blankush JL, Gangeness DE Effect of treatment of Helicobacter pylori infection on rosacea Arch Dermatol 1999; 135: 659-663
75. Kusters JG, Kuipers EJ Helicobacter and atherosclerosis. Am Heart J 1999; 138: S523–527
76. Leontiades GI, Sharma VK, Howden CW Non-gastrointestinal tract associations of Helicobacter pylori infection: what is the evidence? Arch Intern Med 1999; 159: 925-940
77. Gasbarrini A, Franceschi F Does H. pylori infection play a role in idiopathic thrombocytopenic purpura and in other autoimmune diseases? Am J Gastroenterol 2005; 100:1271-1273
78. Jackson S, Beck PL, Pineo GF, Poon MC Helicobacter pylori eradication: novel therapy for immune thrombocytopenic purpura? A review of the literature Am J Hematol 2005; 78: 142-150
79. Suzuki T, Matsushima M, Masui A, Watanabe K, Takagi A, Ogawa Y, Shirai T, Mine T Effect of Helicobacter pylori eradication in patients with chronic idiopathic thrombocytopenic purpura-a randomized controlled trial. Am J Gastroenterol 2005; 100: 1265-1270
80. Arnold IC, Dehzad N, Reuter S, Martin H, Becher B, Taube C, Muller A. Helicobacter pylori infection prevents allergic asthma in mouse models through the induction of regulatory T cells J Clin Invest 2011; 121: 3088-3093
81. 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
82. Feydt-Schmidt A, Russmann H, Lehn N, Fischer A, Antoni I, Stork D, et al. Fluorescence in situ hybridization vs. epsilometer test for detection of clarithromycin-susceptible and clarithromycin-resistant Helicobacter pylori strains in gastric biopsies from children. Aliment Pharmacol Ther 2002; 16[12]: 2073-2079
83. Ni YH, Lin JT, Huang SF, Yang JC, Chang MH. Accurate diagnosis of Helicobacter pylori infection by stool antigen test and 6 other currently available tests in children [see comments]. J Pediatr 2000; 136[6]: 823-827
84. Borrelli O, Hassall E, D'Armiento F, Bosco S, Mancini V, Di Nardo G, et al. Inflammation of the gastric cardia in children with symptoms of acid peptic disease. J Pediatr 2003; 143[4]: 520-524
85. Qualia CM, Katzman PJ, Brown MR, Kooros K. A report of two children with Helicobacter heilmannii gastritis and review of the literature. Pediatr Dev Pathol 2007; 10[5]: 391-394
86. Logan RP Urea breath tests in the management of Helicobacter pylori infection Gut 1998; 43 [Suppl 1]: S47–S50
87. van Doorn OJ, Bosman DK, van't Hoff BW, Taminiau JA, ten Kate FJ, van der Ende A Helicobacter pylori Stool Antigen test: a reliable non-invasive test for the diagnosis of Helicobacter pylori infection in children. Eur J Gastroenterol Hepatol 2001; 13[9]: 1061-1065
88. Ballam LD, Mendall MA, Asante M, Morris J, Strachan DP, Whincup PH, Cook DG. 2000. Western blotting is useful in the salivary diagnosis of Helicobacter pylori infection J Clin Pathol 2000; 53: 314-317
89. De Pascalis R, Del Pezzo M, Nardone G, Budillon G, Lavitola A Performance characteristics of an enzyme-linked immunosorbent assay for determining salivary immunoglobulin G response to Helicobacter pylori J Clin. Microbiol 1999; 37: 430-432
90. Luzza F, Oderda G, Maletta M, Imeneo M, Mesuraca L, Chioboli E, Lerro P, Guandalini S, Pallone F Salivary immunoglobulin G assay to diagnose Helicobacter pylori infection in children  J Clin Microbiol 1997; 35: 3358-3360
91. Luzza F, Maletta M, Imeneo M, Doldo P, Marasco R, Biancone L, Pallone F Salivary specific IgG is a sensitive indicator of the humoral immune response to Helicobacter pylori FEMS Immunol Med Microbiol 1995; 10:281-284
92. Marshall B, Howat AJ, Wright PA Oral fluid antibody detection in the diagnosis of Helicobacter pylori infection J Med Microbiol 1999; 48: 1043-1046
93. Bode G, Marchildon P, Peacock J, Brenner H, Rothenbacher D Diagnosis of Helicobacter pylori Infection in Children: Comparison of a Salivary Immunoglobulin G Antibody Test with the [13C] Urea Breath Test Clin Vaccine Immunol 2002; 9: 493-495
94. Jones NL, Sherman P, Fallone CA, Flook N, Smaill F, van Zanten SV 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[7]: 399-408
95. Talley NJ, Fock KM, Moayyedi P. Gastric cancer consensus conference recommends Helicobacter pylori screening and treatment in asymptomatic persons from high-risk populations to prevent gastric cancer. American Journal of Gastroenterology 2008; 103: 510-514
96. Megraud F, Lehours P Helicobacter pylori detection and antimicrobial susceptibility testing. Clinical Microbiology Review 2007; 20: 280-283
97. Graham DY, Opekun AR, Klein PD Clarithromycin for the eradication of Helicobacter pylori J Clin Gastroenterol 1993; 16: 292-294
98. Peterson WL, Graham DY, Marshall B, Blaser MJ, Genta RM, Klein PD, Stratton CW, Drnec J, Prokocimer P, Siepman N Clarithromycin as monotherapy for eradication of Helicobacter pylori: a randomized, double-blind trial Am J Gastroenterol 1993; 88: 1860-1864
99. Gottrand F, Kalach N, Spyckerelle C, Guimber D, Mougenot JF, Tounian P et al Omeprazole combined with amoxicillin and clarithromycin in the eradication of Helicobacter pylori in children with gastritis: A prospective randomized double-blind trial J Pediatr 2001; 139[5]: 664-668
100. Drumm B, Koletzko S, Oderda G Helicobacter pylori infection in children: A consensus statement J Pediatr Gastroenterol Nutr 2000; 30:207-213
101. Gold B, Colletti RB, Abbott M, Czinn S, Elitsur Y, Hassall E et al Medical Position Paper: The North American Society for Pediatric Gastroenterology and Nutrition: Helicobacter pylori infection in children: Recommendations for diagnosis and treatment J Pediatr Gastroenterol Nutr 2000; 31: 490-497
102. Oderda G, Shcherbakov P, Bontems P, Urruzuno P, Romano C, Gottrand F et al Results from the pediatric European register for treatment of Helicobacter pylori [PERTH] Helicobacter 2007; 12(2): 150-156
103. Graham DY, Fischbach L Helicobacter pylori treatment in the era of increasing antibiotic resistance. Gut 2010; 59(8): 1143-1153
104. Kalach N, Benhamou PH, Campeotto F, Bergeret M, Dupont C, Raymond J Clarithromycin resistance and bacterial eradication of Helicobacter pylori in children Antimicrob Agents Chemother 2001; 45: 2134-2135
105. Gisbert JP, Calvet X, O'Connor A, Megraud F, O'Morain CA. Sequential therapy for Helicobacter pylori eradication: a critical review J Clin Gastroenterol 2010; 44(5): 313-325
106. Arenz T, Antos D, Russmann H, Alberer M, Buderus S, Kappler M, et al. Esomeprazole-based 1-week triple therapy directed by susceptibility testing for eradication of Helicobacter pylori infection in children. J Pediatr Gastroenterol Nutr 2006; 43[2]: 180-184
107. Street M, Cellini L, Di Campli E, Magliani W, Manfredi M, Fornaroli F, et al. Antibiotic resistance and antibiotic sensitivity based treatment in Helicobacter pylori infection: advantages and outcome Arch Dis Child 2001; 84: 419-422
108. Faber J, BarMeir M, Rudensky B, Schlesinger Y, Rachman E, Benenson S et al Treatment regimens for Helicobacter pylori infection in children: is in vitro susceptibility testing helpful? J Pediatr Gastroenterol Nutr 2005; 40(5): 571-574
109. O’Connor A, Gisbert JP, McNamara D, Morain CO. Treatment of Helicobacter pylori infection 2011; 16 (S1): 53-58
110. Lionetti E, Indrio F, Lorenzo P, Borrelli G, Cavallo L, Francavilla R. Role of probiotics in pediatric patients with Helicobacter pylori infection: A comprehensive review of the literature. Helicobacter 2010; 15 (2): 79-87
111. Armstrong JA, Wee SH, Goodwin CS, Wilson DH Response of Campylobacter pyloridis to antibiotics, bismuth and an acid reducing agent in vitro-an ultrastructural study J Med Microbiol 1987; 24: 343-350
112. Lambert JR, Midolo P The actions of bismuth in the treatment of Helicobacter pylori infection Aliment Pharmacol Ther 1997; 11: 27-33
113. Vogt K, Warrelmann M, Hahn H The minimum inhibitory concentrations of various bismuth salts against Campylobacter pylori Zentbl Bakteriol 1989; 271: 304-308
114. Megraud F, Lamouliatte H Review article: the treatment of refractory Helicobacter pylori infection. Aliment Pharmacol Ther 2003; 17: 1333-1343
115. Perri F, Festa V, Andriulli A Treatment of antibiotic-resistant Helicobacter pylori N Engl J Med 1998; 339: 53
116. Perri F, Festa V, Clemente R, Quitadamo M, Andriulli A Rifabutin-based ‘rescue therapy’ for Helicobacter pylori infected patients after failure of standard regimens Aliment Pharmacol Ther 2000; 14: 311-316
117. Ebrahimi-Dariani N, Mirmomen S, Mansour-Ghanaei F, Noormohammadpoor P, Sotodehmanesh R, Haghpanah B, Bahrami H The efficacy of furazolidone-based quadruple therapy for eradication of Helicobacter pylori infection in Iranian patients resistant to metronidazolebased quadruple therapy Med Sci Monit 2003; 9: PI105-PI108
118. Fakheri H, Merat S, Hosseini V, Malekzadeh R Low-dose furazolidone in triple and quadruple regimens for Helicobacter pylori eradication Aliment Pharmacol Ther 2004; 19: 89-93
119. Xiao SD,  Liu WZ, Xia DH, Jiang SJ, Wang RN, Zhang ZH, and Xu WW The efficacy of furazolidone and metronidazole in the treatment of chronic gastritis associated with Helicobacter (Campylobacter) pylori-a randomized double-blind placebo-controlled clinical trial. HepatoGastroenterology 1990; 37: 503-506
120. Dresner D, Coyle W, Nemec R, Peterson R, Duntemann T, Lawson JM Efficacy of ciprofloxacin in the eradication of Helicobacter pylori South Med J 1996; 89: 775-778
121. Forsmark CE, Wilcox CM, Cello JP, Margaretten W, Lee B, Sachdeeva M, Satow J, Sande MA Ciprofloxacin in the treatment of Helicobacter pylori in patients with gastritis and peptic ulcer J Infect Dis 1990; 162: 998-999
122. Sanaka M., Kuyama Y, Yamanaka M, Iwasaki M Decrease in serum concentrations of Helicobacter pylori IgG antibodies during antituberculosis therapy: the possible eradication by rifampicin and streptomycin Am J Gastroenterol 1999;  94: 1983-1984
123. Khurana R, Fischbach L, Chiba N, van Zanten SV, Sherman PM, George BA et al. Meta-analysis: Helicobacter pylori eradication treatment efficacy in children. Aliment Pharmacol Ther 2007; 25(5): 523-536
124. Hoffelner H, Rieder G, Haas R Helicobacter pylori vaccine development: optimisation of strategies and importance of challenging strain and animal model International Journal of Medical Microbiology 2008; 298 (1-2): 151-159
125. Kabir S The current status of Helicobacter pylori vaccines: a review Helicobacter 2007; 12 (2): 89-102
126. Malfertheiner P, Schultze V, Rosenkranz B Safety and Immunogenicity of an intramuscular Helicobacter pylori Vaccine in non-infected Volunteers: A Phase I Study Gastroenterology 2008; 135 (3): 787-795
127. Kabir S. The current status of Helicobacter pylori vaccines: A review Helicobacter 2007; 12 (2): 89-102

Source(s) of Funding


Competing Interests



This article has been downloaded from WebmedCentral. With our unique author driven post publication peer review, contents posted on this web portal do not undergo any prepublication peer or editorial review. It is completely the responsibility of the authors to ensure not only scientific and ethical standards of the manuscript but also its grammatical accuracy. Authors must ensure that they obtain all the necessary permissions before submitting any information that requires obtaining a consent or approval from a third party. Authors should also ensure not to submit any information which they do not have the copyright of or of which they have transferred the copyrights to a third party.
Contents on WebmedCentral are purely for biomedical researchers and scientists. They are not meant to cater to the needs of an individual patient. The web portal or any content(s) therein is neither designed to support, nor replace, the relationship that exists between a patient/site visitor and his/her physician. Your use of the WebmedCentral site and its contents is entirely at your own risk. We do not take any responsibility for any harm that you may suffer or inflict on a third person by following the contents of this website.

3 reviews posted so far

Review on H.Pylori In Children
Posted by Dr. Sameeh S Ghazal on 29 Aug 2012 06:03:09 AM GMT

Dear Dr. Sameeh Ghazal, Thank u so much for your valuable suggestions. They have been noted and will be incorporated in the revision of the ms TQ Best rgds Dr. Shahid... View more
Responded by Dr. Sukhbir Shahid on 30 Aug 2012 05:41:52 AM GMT

H Pylori Infection is Not Necessarily Bad News
Posted by Dr. Jacob Puliyel on 27 Aug 2012 12:23:12 AM GMT

Dear Dr. J Puliyel, Thank you so much for your suggestions to improve my article. The points have been noted and will be incorporated in my revised ms. TQ Best rgds Dr. Shahid SK... View more
Responded by Dr. Sukhbir Shahid on 27 Aug 2012 04:55:58 PM GMT

Of Mice and Men (& Children)
Posted by Dr. Israel Kochin on 24 Aug 2012 03:15:58 PM GMT

Dear Dr. Israel Kochin, Thanks for your comments. Will look into the suggested points while revising my script TQ Best rgds Dr. Shahid... View more
Responded by Dr. Sukhbir Shahid on 26 Aug 2012 05:17:40 AM GMT

2 comments posted so far

review comment Posted by Dr. Sameeh S Ghazal on 26 Aug 2012 08:16:17 AM GMT

Dear Dr. Sameeh Ghazal, Thanks for taking time to review and comment on my article. The points are well taken and will be incorporated in the revised version of the ms TQ Best rgds Dr. Shahid SK. ... View more
Responded by Dr. Sukhbir Shahid on 26 Aug 2012 08:30:09 AM GMT

Dear Dr. Rajan, Thanks for your comments. Points are noted and will be included in revised version of ms TQ Best rgds Dr. Shahid S. ... View more
Responded by Dr. Sukhbir Shahid on 26 Aug 2012 08:32:35 AM GMT

Please use this functionality to flag objectionable, inappropriate, inaccurate, and offensive content to WebmedCentral Team and the authors.


Author Comments
0 comments posted so far


What is article Popularity?

Article popularity is calculated by considering the scores: age of the article
Popularity = (P - 1) / (T + 2)^1.5
P : points is the sum of individual scores, which includes article Views, Downloads, Reviews, Comments and their weightage

Scores   Weightage
Views Points X 1
Download Points X 2
Comment Points X 5
Review Points X 10
Points= sum(Views Points + Download Points + Comment Points + Review Points)
T : time since submission in hours.
P is subtracted by 1 to negate submitter's vote.
Age factor is (time since submission in hours plus two) to the power of 1.5.factor.

How Article Quality Works?

For each article Authors/Readers, Reviewers and WMC Editors can review/rate the articles. These ratings are used to determine Feedback Scores.

In most cases, article receive ratings in the range of 0 to 10. We calculate average of all the ratings and consider it as article quality.

Quality=Average(Authors/Readers Ratings + Reviewers Ratings + WMC Editor Ratings)