Comparison of acid outputs (mMol/h between infected and non-infected children along with effect of anti-
1. Introduction
At least half the world's population are infected by
In this chapter, we will review and update the consequence of
2. Consequences of initial H. pylori infection in children
There are not enough studies on the natural history of gastric infections in childhood years. In older children and adolescents, and adults it appears that
Some studies reported pan-gastritis involving both body and antrum in children infected with
2.1. H. pylori infection and gastric acid perturbation
Acid secretion by the gastric parietal cell is regulated by paracrine, endocrine, and neural pathways. The physiological stimuli for acid secretion include histamine, acetylcholine, and gastrin, each of which binds to receptors located on the basolateral plasma membranes of the cells. The antral region of stomach contains G cells which release hormone gastrin. When meal is ingested, the protein component stimulates G cell to release Gastrin, which travels through the bloodstream to parietal cells in the body region (fundus) to secret acid [25]. Gastrin directly does not stimulate parietal cells but stimulates the adjacent enterochromafin-like cell (ECL cells) to release histamine, which in turn stimulates the parietal cells. Stimulation of acid secretion typically involves an activation of a cAMP-dependent protein kinase cascade that triggers the translocation and insertion of the proton pump enzyme, H,K-ATPase, into the apical plasma membrane parietal cells [26]. As the acid accumulates and overcome the buffering effects of the food, the fall in intragastric pH inhibits further release of gastrin and thus prevents secretion of excessive amount of acids (negative feedback control).
2.2. H. pylori infection and increased acid output (hyperchlorhydria)
2.3. H. pylori infection and low acid output (hypochlorhydria)
In subjects with atrophic gastritis or body predominant gastritis, there also is increased gastrin release, but that is not accompanied with increased acid secretion. In such subjects, acid secretion is reduced or completely absent (achlorhydria) [36, 37]. The low acid secretion, despite increased gastrin levels, indicates markedly impaired ability of oxyntic mucosa to secret acid in response to gastrin. Following eradication of
3. Role of H. pylori infection in gastric acid perturbation in children
There are only a few pediatric case reports on gastric acid secretion in
|
|
|
|
||
Basal Acid Output (BAO) | 0.23 ± 0.30 | 0.06 | 0.62 ±0.9 | NS | 0.65 ± 0.65 |
Stimulated Acid Output | 2.04 ±1.4 | 0.001 | 3.4 ±2.5 | NS | 3.3 ±2.1 |
4. Potential mechanisms of H. pylori -induced hypochlorhydria
An alternative explanation for the impaired acid secretory function is infection-induced inflammation of the oxyntic mucosa, since the severity of inflammation of the body mucosa is more marked in subjects with
The molecular mechanisms underlying
4.1. Potential consequences of H. pylori induced hypochlorhydria
5. H. pylori infection and iron deficiency anemia
5.1. Iron deficiency and iron deficiency anemia
Iron deficiency (ID) and iron deficiency anemia (IDA) are major public health problems, especially in children and women of childbearing age in developing countries [52], and is considered one of the ten leading global risks factors in terms of its attributable disease burden [53]. It has been estimated that globally approximately 1.6 billion people, representing 25% of the total population are anemic [54]. ID is considered to account for 50% of identified anemia, and 800,000 deaths worldwide can be attributed to IDA. Deficiency of this trace element has adverse implications on health at all stages of life. When iron deficiency occurs during critical windows of brain development, the resultant cognitive deficits may be irreversible and unresponsive to subsequent improvements in the iron status [55]. In adults, ID and IDA can adversely impact physical work capacity and work productivity - variables that may have a detrimental impact on their economic potential [56].
5.2. H. pylori and iron deficiency anemia
Several reports have demonstrated an association between
In Bangladesh, a randomized controlled community based study was conducted to determine whether or not
The results of the study indicated that iron status, as reevaluated on day-90, improved in all groups. However, the improvement was significantly higher among 3 groups receiving iron (anti-
5.3. H. pylori and iron absorption
Non-heme iron absorption requires an acidic milieu. Non-water-soluble iron compounds, e.g. ferrous and ferric pyrophosphate are often used in the fortification programs because they cause no unacceptable organoleptic changes in the fortified food. However, these compounds need gastric acid for their solubilization and absorption. Therefore, if gastric acid output is compromised as a consequence of
|
|
|
|||||||
|
|
|
|
|
|
|
|
|
|
% | % | % | |||||||
Geometric mean | 5.3 | 19.7 | 26.9 | 6.4 | 22.5 | 28.3 | 5.4 | 15.6 | 34.8 |
+1SD | 13.5 | 32.9 | 49.0 | 12.9 | 33.0 | 47.7 | 12.7 | 30.1 | 64.3 |
-1SD | 2.1 | 11.8 | 14.8 | 3.2 | 15.4 | 16.8 | 2.3 | 8.1 | 18.8 |
|
<0.0001 | <0.0001 | <0.001 | ||||||
1P value for iron absorption from ferrous fumarate compared with that from ferrous sulfate within each group. |
5.3.1. Mechanism of IDA
The interaction between
5.4. H. pylori and vitamin C
Ascorbic acid is the reduced form of the vitamin, which can act as a potent antioxidant for neutralizing nitrite-derived mutagens protecting against gastric carcinogenesis [90]. Vitamin C is first absorbed and then is actively secreted, mainly in the antral mucosa, from plasma into gastric juice. Once there, it is able to react with nitrosating agents preventing N-nitroso compounds formation; however, vitamin C in the stomach interacts with iron improving its absorption. In children
In developing countries, low intake of vitamin C-enriched food is associated with higher prevalence of
6. Conclusion
The combination of micronutrient deficiency and more frequent enteric infections consequent to
Acknowledgments
I gratefully acknowledge Dr. Mohammed Abdus Salam, Director, Research & Clinial Administration and Strategy, icddr,b for his review and valuable comments.
References
- 1.
Pounder, R.E. and D. Ng, The prevalence of Helicobacter pylori infection in different countries. Aliment Pharmacol Ther, 1995. 9 Suppl 2: p. 33-9. - 2.
Malaty, H.M., et al., Helicobacter pylori in Hispanics: comparison with blacks and whites of similar age and socioeconomic class. Gastroenterology, 1992. 103(3): p. 813-6. - 3.
Mitchell, H.M., et al., Epidemiology of Helicobacter pylori in southern China: identification of early childhood as the critical period for acquisition. J Infect Dis, 1992. 166(1): p. 149-53. - 4.
Goh, K.L., Prevalence of and risk factors for Helicobacter pylori infection in a multi-racial dyspeptic Malaysian population undergoing endoscopy. J Gastroenterol Hepatol, 1997. 12(6): p. S29-35. - 5.
Graham, D.Y., et al., Seroepidemiology of Helicobacter pylori infection in India. Comparison of developing and developed countries. Dig Dis Sci, 1991. 36(8): p. 1084-8. - 6.
Kehrt, R., et al., Prevalence of Helicobacter pylori infection in Nicaraguan children with persistent diarrhea, diagnosed by the 13C-urea breath test. J Pediatr Gastroenterol Nutr, 1997. 25(1): p. 84-8. - 7.
Sarker, S.A., et al., Prevalence of Helicobacter pylori infection in infants and family contacts in a poor Bangladesh community. Dig Dis Sci, 1995. 40(12): p. 2669-72. - 8.
Thomas, J.E., et al., Early Helicobacter pylori colonisation: the association with growth faltering in The Gambia. Arch Dis Child, 2004. 89(12): p. 1149-54. - 9.
HM., M., Epidemiology of Infection.. In: Mobley HLT, Mendz GL, Hazell SL, editors. Helicobacter pylori: Physiology and Genetics. Washington (DC): ASM Press; 2001. Chapter 2. Available from: http://www.ncbi.nlm.nih.gov/books/NBK2421/, 2001. - 10.
Kusters, J.G., A.H. van Vliet, and E.J. Kuipers, Pathogenesis of Helicobacter pylori infection. Clin Microbiol Rev, 2006. 19(3): p. 449-90. - 11.
McColl, K.E., E. el-Omar, and D. Gillen, Interactions between H. pylori infection, gastric acid secretion and anti-secretory therapy. Br Med Bull, 1998. 54(1): p. 121-38. - 12.
Leontiadis, G.I., V.K. Sharma, and C.W. Howden, Non-gastrointestinal tract associations of Helicobacter pylori infection. Arch Intern Med, 1999. 159(9): p. 925-40. - 13.
Yip, R., et al., Pervasive occult gastrointestinal bleeding in an Alaska native population with prevalent iron deficiency. Role of Helicobacter pylori gastritis. Jama, 1997. 277(14): p. 1135-9. - 14.
Malaty, H.M., et al., Natural history of Helicobacter pylori infection in childhood: 12-year follow-up cohort study in a biracial community. Clin Infect Dis, 1999. 28(2): p. 279-82. - 15.
Tindberg, Y., M. Blennow, and M. Granstrom, Clinical symptoms and social factors in a cohort of children spontaneously clearing Helicobacter pylori infection. Acta Paediatr, 1999. 88(6): p. 631-5. - 16.
Perri, F., et al., Helicobacter pylori infection may undergo spontaneous eradication in children: a 2-year follow-up study. J Pediatr Gastroenterol Nutr, 1998. 27(2): p. 181-3. - 17.
Sarker, S.A., et al., Helicobacter pylori: prevalence, transmission, and serum pepsinogen II concentrations in children of a poor periurban community in Bangladesh. Clin Infect Dis, 1997. 25(5): p. 990-5. - 18.
Bahu Mda, G., et al., Endoscopic nodular gastritis: an endoscopic indicator of high-grade bacterial colonization and severe gastritis in children with Helicobacter pylori. J Pediatr Gastroenterol Nutr, 2003. 36(2): p. 217-22. - 19.
Gottrand, F., et al., Normal gastric histology in Helicobacter pylori-infected children. J Pediatr Gastroenterol Nutr, 1997. 25(1): p. 74-8. - 20.
Baysoy, G., et al., Gastric histopathology, iron status and iron deficiency anemia in children with Helicobacter pylori infection. J Pediatr Gastroenterol Nutr, 2004. 38(2): p. 146-51. - 21.
Queiroz, D.M., et al., Differences in distribution and severity of Helicobacter pylori gastritis in children and adults with duodenal ulcer disease. J Pediatr Gastroenterol Nutr, 1991. 12(2): p. 178-81. - 22.
Dohil, R., et al., Gastritis and gastropathy of childhood. J Pediatr Gastroenterol Nutr, 1999. 29(4): p. 378-94. - 23.
Kato, S., et al., Long-term follow-up study of serum immunoglobulin G and immunoglobulin A antibodies after Helicobacter pylori eradication. Pediatrics, 1999. 104(2): p. e22. - 24.
Ganga-Zandzou, P.S., et al., Natural outcome of Helicobacter pylori infection in asymptomatic children: a two-year follow-up study. Pediatrics, 1999. 104(2 Pt 1): p. 216-21. - 25.
Blaser, M.J. and J.C. Atherton, Helicobacter pylori persistence: biology and disease. J Clin Invest, 2004. 113(3): p. 321-33. - 26.
Yao, X. and J.G. Forte, Cell biology of acid secretion by the parietal cell. Annu Rev Physiol, 2003. 65: p. 103-31. - 27.
Sobala, G.M., et al., Acute Helicobacter pylori infection: clinical features, local and systemic immune response, gastric mucosal histology, and gastric juice ascorbic acid concentrations. Gut, 1991. 32(11): p. 1415-8. - 28.
Iijima, K., et al., Changes in gastric acid secretion assayed by endoscopic gastrin test before and after Helicobacter pylori eradication. Gut, 2000. 46(1): p. 20-6. - 29.
McColl, K.E., E. el-Omar, and D. Gillen, Helicobacter pylori gastritis and gastric physiology. Gastroenterol Clin North Am, 2000. 29(3): p. 687-703, viii. - 30.
Louw, J.A., et al., Distribution of Helicobacter pylori colonisation and associated gastric inflammatory changes: difference between patients with duodenal and gastric ulcers. J Clin Pathol, 1993. 46(8): p. 754-6. - 31.
Levi, S., et al., Campylobacter pylori and duodenal ulcers: the gastrin link. Lancet, 1989. 1(8648): p. 1167-8. - 32.
McColl, K.E., et al., Plasma gastrin, daytime intragastric pH, and nocturnal acid output before and at 1 and 7 months after eradication of Helicobacter pylori in duodenal ulcer subjects. Scand J Gastroenterol, 1991. 26(3): p. 339-46. - 33.
el-Omar, E., et al., Eradicating Helicobacter pylori infection lowers gastrin mediated acid secretion by two thirds in patients with duodenal ulcer. Gut, 1993. 34(8): p. 1060-5. - 34.
Harris, A.W., et al., Eradication of Helicobacter pylori in patients with duodenal ulcer lowers basal and peak acid outputs to gastrin releasing peptide and pentagastrin. Gut, 1996. 38(5): p. 663-7. - 35.
Hamlet, A. and L. Olbe, The influence of Helicobacter pylori infection on postprandial duodenal acid load and duodenal bulb pH in humans. Gastroenterology, 1996. 111(2): p. 391-400. - 36.
El-Omar, E.M., et al., Helicobacter pylori infection and chronic gastric acid hyposecretion. Gastroenterology, 1997. 113(1): p. 15-24. - 37.
Gutierrez, O., et al., Cure of Helicobacter pylori infection improves gastric acid secretion in patients with corpus gastritis. Scand J Gastroenterol, 1997. 32(7): p. 664-8. - 38.
Euler, A.R., et al., Basal and pentagstrin-stimulated gastric acid secretory rates in normal children and in those with peptic ulcer disease. J Pediatr, 1983. 103: p. 766-8. - 39.
Christie, D.L. and M.E. Ament, Gastric acid hypersecretion in children with duodenal ulcer. Gastroenterology, 1976. 71(2): p. 242-4. - 40.
Kato, S., et al., Effect of Helicobacter pylori infection on gastric acid secretion and meal-stimulated serum gastrin in children. Helicobacter, 2004. 9(2): p. 100-5. - 41.
Sarker, S.A., et al., Influence of Helicobacter pylori infection on gastric acid secretion in pre-school Bangladeshi children. Helicobacter. 17(5): p. 333-9. - 42.
Sachs, G., Gastritis, Helicobacter pylori, and proton pump inhibitors. Gastroenterology, 1997. 112(3): p. 1033-6. - 43.
Gillen, D., et al., Helicobacter pylori infection potentiates the inhibition of gastric acid secretion by omeprazole. Gut, 1999. 44(4): p. 468-75. - 44.
El-Omar, E.M., et al., Increased prevalence of precancerous changes in relatives of gastric cancer patients: critical role of H. pylori. Gastroenterology, 2000. 118(1): p. 22-30. - 45.
Furuta, T., et al., Interleukin 1beta polymorphisms increase risk of hypochlorhydria and atrophic gastritis and reduce risk of duodenal ulcer recurrence in Japan. Gastroenterology, 2002. 123(1): p. 92-105. - 46.
Wallace, J.L., et al., Secretagogue-specific effects of interleukin-1 on gastric acid secretion. Am J Physiol, 1991. 261(4 Pt 1): p. G559-64. - 47.
Windle, H.J., D. Kelleher, and J.E. Crabtree, Childhood Helicobacter pylori infection and growth impairment in developing countries: a vicious cycle? Pediatrics, 2007. 119(3): p. e754-9. - 48.
Furuta, T., et al., Effect of Helicobacter pylori infection on gastric juice pH. Scand J Gastroenterol, 1998. 33(4): p. 357-63. - 49.
Wang, F., et al., Helicobacter pylori VacA disrupts apical membrane-cytoskeletal interactions in gastric parietal cells. J Biol Chem, 2008. 283(39): p. 26714-25. - 50.
Gilman, R.H., et al., Decreased gastric acid secretion and bacterial colonization of the stomach in severely malnourished Bangladeshi children. Gastroenterology, 1988. 94(6): p. 1308-14. - 51.
Vitale, G., et al., Nutritional aspects of Helicobacter pylori infection. Minerva Gastroenterol Dietol. 57(4): p. 369-77. - 52.
McLean, E., et al., Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993-2005. Public Health Nutr, 2008: p. 1-11. - 53.
WHO, The World Health Report 2002: Reducing risks, promoting healthy life. 2002, Geneva: World Health Organization. - 54.
McLean, E., et al., Worldwide prevalence of anaemia, WHO Vitamin and Mineral Nutrition Information System, 1993-2005. Public Health Nutr, 2009. 12(4): p. 444-54. - 55.
Beard, J.L., Why iron deficiency is important in infant development. J Nutr, 2008. 138(12): p. 2534-6. - 56.
WHO and UNICEF (2004) Focusing on anaemia; towards an integrated approach for effective anaemia control. Volume, - 57.
Seo, J.K., J.S. Ko, and K.D. Choi, Serum ferritin and Helicobacter pylori infection in children: a sero-epidemiologic study in Korea. J Gastroenterol Hepatol, 2002. 17(7): p. 754-7. - 58.
Kostaki, M., S. Fessatou, and T. Karpathios, Refractory iron-deficiency anaemia due to silent Helicobacter pylori gastritis in children. Eur J Pediatr, 2003. 162(3): p. 177-9. - 59.
Marignani, M., et al., Reversal of long-standing iron deficiency anaemia after eradication of Helicobacter pylori infection. Scand J Gastroenterol, 1997. 32(6): p. 617-22. - 60.
Cardenas, V.M., et al., Iron deficiency and Helicobacter pylori infection in the United States. Am J Epidemiol, 2006. 163(2): p. 127-34. - 61.
Annibale, B., et al., Reversal of iron deficiency anemia after Helicobacter pylori eradication in patients with asymptomatic gastritis. Ann Intern Med, 1999. 131(9): p. 668-72. - 62.
Choe, Y.H., et al., Randomized placebo-controlled trial of Helicobacter pylori eradication for iron-deficiency anemia in preadolescent children and adolescents. Helicobacter, 1999. 4(2): p. 135-9. - 63.
Russo-Mancuso, G., et al., Iron deficiency anemia as the only sign of infection with Helicobacter pylori: a report of 9 pediatric cases. Int J Hematol, 2003. 78(5): p. 429-31. - 64.
Hershko, C., et al., Role of autoimmune gastritis, Helicobacter pylori and celiac disease in refractory or unexplained iron deficiency anemia. Haematologica, 2005. 90(5): p. 585-95. - 65.
Bergamschi, G., Role of autoimmune gastritis, Helicobacter pylori and celiac disease in refractory or unexplained iron deficiency anemia. Hematologica, 2005. 90: p. 577A. - 66.
Barabino, A., et al., Unexplained refractory iron-deficiency anemia associated with Helicobacter pylori gastric infection in children: further clinical evidence. J Pediatr Gastroenterol Nutr, 1999. 28(1): p. 116-9. - 67.
Ashorn, M., T. Ruuska, and A. Makipernaa, Helicobacter pylori and iron deficiency anaemia in children. Scand J Gastroenterol, 2001. 36(7): p. 701-5. - 68.
Malfertheiner, P., et al., Current concepts in the management of Helicobacter pylori infection: the Maastricht III Consensus Report. Gut, 2007. 56(6): p. 772-81. - 69.
Iijima, K., et al., Gastric acid secretion of normal Japanese subjects in relation to Helicobacter pylori infection, aging, and gender. Scand J Gastroenterol, 2004. 39(8): p. 709-16. - 70.
Rokkas, T., et al., Helicobacter pylori infection and gastric juice vitamin C levels. Impact of eradication. Dig Dis Sci, 1995. 40(3): p. 615-21. - 71.
Annibale, B., et al., Concomitant alterations in intragastric pH and ascorbic acid concentration in patients with Helicobacter pylori gastritis and associated iron deficiency anaemia. Gut, 2003. 52(4): p. 496-501. - 72.
Husson, M.O., et al., Iron acquisition by Helicobacter pylori: importance of human lactoferrin. Infect Immun, 1993. 61(6): p. 2694-7. - 73.
Sarker, S.A., et al., Causal relationship of Helicobacter pylori with iron-deficiency anemia or failure of iron supplementation in children. Gastroenterology, 2008. 135(5): p. 1534-42. - 74.
Dallman, P., Laboratory diagnosis of iron deficiency in infancy and early childhood. Annales Nestle, 1995. 53: p. 18-24. - 75.
Muhsen, K. and D. Cohen, Helicobacter pylori infection and iron stores: a systematic review and meta-analysis. Helicobacter, 2008. 13(5): p. 323-40. - 76.
Qu, X.H., et al., Does Helicobacter pylori infection play a role in iron deficiency anemia? A meta-analysis. World J Gastroenterol. 16(7): p. 886-96. - 77.
Huang, X., et al., Iron deficiency anaemia can be improved after eradication of Helicobacter pylori. Postgrad Med J. 86(1015): p. 272-8. - 78.
Yuan, W., et al., Iron deficiency anemia in Helicobacter pylori infection: meta-analysis of randomized controlled trials. Scand J Gastroenterol. 45(6): p. 665-76. - 79.
Sarker, S.A., et al., Helicobacter pylori infection, iron absorption, and gastric acid secretion in Bangladeshi children. Am J Clin Nutr, 2004. 80(1): p. 149-53. - 80.
Kastenmayer, P., et al., A double stable isotope technique for measuring iron absorption in infants. Br J Nutr, 1994. 71(3): p. 411-24. - 81.
Carrizo-Chavez, M.A., A. Cruz-Castaneda, and J. Olivares-Trejo Jde, The frpB1 gene of Helicobacter pylori is regulated by iron and encodes a membrane protein capable of binding haem and haemoglobin. FEBS Lett. 586(6): p. 875-9. - 82.
Keenan, J.I., et al., The effect of Helicobacter pylori infection and dietary iron deficiency on host iron homeostasis: a study in mice. Helicobacter, 2004. 9(6): p. 643-50. - 83.
Yokota, S., et al., Enhanced Fe ion-uptake activity in Helicobacter pylori strains isolated from patients with iron-deficiency anemia. Clin Infect Dis, 2008. 46(4): p. e31-3. - 84.
Luqmani, Y.A., et al., Expression of lactoferrin in human stomach. Int J Cancer, 1991. 49(5): p. 684-7. - 85.
Dhaenens, L., F. Szczebara, and M.O. Husson, Identification, characterization, and immunogenicity of the lactoferrin-binding protein from Helicobacter pylori. Infect Immun, 1997. 65(2): p. 514-8. - 86.
Nakao, K., et al., Relation of lactoferrin levels in gastric mucosa with Helicobacter pylori infection and with the degree of gastric inflammation. Am J Gastroenterol, 1997. 92(6): p. 1005-11. - 87.
Senkovich, O., et al., Unique host iron utilization mechanisms of Helicobacter pylori revealed with iron-deficient chemically defined media. Infect Immun. 78(5): p. 1841-9. - 88.
Worst, D.J., B.R. Otto, and J. de Graaff, Iron-repressible outer membrane proteins of Helicobacter pylori involved in heme uptake. Infect Immun, 1995. 63(10): p. 4161-5. - 89.
Block, G., Vitamin C and cancer prevention: the epidemiologic evidence. Am J Clin Nutr, 1991. 53(1 Suppl): p. 270S-282S. - 90.
Zhang, Z.W., M. Abdullahi, and M.J. Farthing, Effect of physiological concentrations of vitamin C on gastric cancer cells and Helicobacter pylori. Gut, 2002. 50(2): p. 165-9. - 91.
Woodward, M., H. Tunstall-Pedoe, and K. McColl, Helicobacter pylori infection reduces systemic availability of dietary vitamin C. Eur J Gastroenterol Hepatol, 2001. 13(3): p. 233-7. - 92.
Odum, L. and L.P. Andersen, Investigation of Helicobacter pylori ascorbic acid oxidating activity. FEMS Immunol Med Microbiol, 1995. 10(3-4): p. 289-94. - 93.
Park, J.H., et al., Correlation between Helicobacter pylori infection and vitamin C levels in whole blood, plasma, and gastric juice, and the pH of gastric juice in Korean children. J Pediatr Gastroenterol Nutr, 2003. 37(1): p. 53-62. - 94.
Mooney, C., et al., Neutrophil activation by Helicobacter pylori. Gut, 1991. 32(8): p. 853-7. - 95.
Frei, B., L. England, and B.N. Ames, Ascorbate is an outstanding antioxidant in human blood plasma. Proc Natl Acad Sci U S A, 1989. 86(16): p. 6377-81. - 96.
Banerjee, S., et al., Effect of Helicobacter pylori and its eradication on gastric juice ascorbic acid. Gut, 1994. 35(3): p. 317-22. - 97.
Jarosz, M., et al., Effects of high dose vitamin C treatment on Helicobacter pylori infection and total vitamin C concentration in gastric juice. Eur J Cancer Prev, 1998. 7(6): p. 449-54. - 98.
Pal, J., M.G. Sanal, and G.J. Gopal, Vitamin-C as anti-Helicobacter pylori agent: More prophylactic than curative- Critical review. Indian J Pharmacol. 43(6): p. 624-7. - 99.
Payne, S.M., Iron acquisition in microbial pathogenesis. Trends Microbiol, 1993. 1(2): p. 66-9. - 100.
Bullen, J.J., C.G. Ward, and H.J. Rogers, The critical role of iron in some clinical infections. Eur J Clin Microbiol Infect Dis, 1991. 10(8): p. 613-7. - 101.
Otto, B.R., A.M. Verweij-van Vught, and D.M. MacLaren, Transferrins and heme-compounds as iron sources for pathogenic bacteria. Crit Rev Microbiol, 1992. 18(3): p. 217-33. - 102.
Ciacci, C., et al., Helicobacter pylori impairs iron absorption in infected individuals. Dig Liver Dis, 2004. 36(7): p. 455-60. - 103.
Azab, S.F. and A.M. Esh, Serum hepcidin levels in Helicobacter pylori-infected children with iron-deficiency anemia: a case-control study. Ann Hematol. 92(11): p. 1477-83.