Advertisement

Current Genetic Medicine Reports

, Volume 6, Issue 4, pp 199–207 | Cite as

Tipping the Scale Towards Gastric Disease: a Host-Pathogen Genomic Mismatch?

  • Gloria Tavera
  • Douglas R. Morgan
  • Scott M. Williams
Genomics (S Williams, Section Editor)
  • 9 Downloads
Part of the following topical collections:
  1. Genomics

Abstract

Purpose of Review

Chronic infection with Helicobacter pylori infection is necessary but not sufficient to initiate development of intestinal-type gastric adenocarcinoma. It is not clear what additional factors tip the scale from commensal bacteria towards a pathogen that facilitates development of gastric cancer. Genetic variants in both the pathogen and host have been implicated, but neither alone explains a substantial portion of disease risk.

Recent Findings

In this review, we consider studies that address the important role of human and bacterial genetics and ancestry and their interactions in determining gastric disease risk. We observe gaps in the current literature that should guide future work to confirm the hypothesis of the interacting roles of host and bacterial genetics that will be necessary to translate these findings into clinically relevant information.

Summary

We summarize genetic risk factors for gastric disease in both H. pylori and human hosts. However, genetic variation of one or the other organism in isolation insufficiently explains gastric disease risk. The most promising models of gastric disease risk simultaneously consider the genetic variation of both the H. pylori and human host, under a co-evolution model.

Keywords

H. pylori Gastric disease Co-evolution Disease risk Genetic ancestry Genome interaction 

Notes

Compliance with Ethical Standards

Conflicts of Interest

The following funding provided support in part:

SMW & DM: US National Institutes of Health grants P30 CA068485 and PAR-15-155 (Vanderbilt Ingram Cancer Center), R01CA190612, and P01CA028842.

GT: Howard Hughes Medical Institute: Gilliam Fellowship, Case Western Reserve University Medical Scientist Training Program T32.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.
    Ferlay J, et al. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer. 2015;136(5):E359–386.PubMedGoogle Scholar
  2. 2.
    Torre LA, et al. Global cancer statistics, 2012. CA Cancer J Clin. 2015;65(2):87–108.CrossRefGoogle Scholar
  3. 3.
    Allemani C, et al. Global surveillance of trends in cancer survival 2000–14 (CONCORD-3): analysis of individual records for 37 513 025 patients diagnosed with one of 18 cancers from 322 population-based registries in 71 countries. Lancet. 2018;391:1023–75.PubMedGoogle Scholar
  4. 4.
    Wroblewski LE, Peek RM Jr, Wilson KT. Helicobacter pylori and gastric cancer: factors that modulate disease risk. Clin Microbiol Rev. 2010;23(4):713–39.PubMedPubMedCentralGoogle Scholar
  5. 5.
    IARC Working Group. IARC monograph on the evaluation of carcinogenic risks to humans: schistosomes, liver flukes and Helicobacter pylori. Lyon: International Agency for Research on Cancer; 1994.Google Scholar
  6. 6.
    Correa P, Piazuelo B. Helicobacter pylori infection and gastric adenocarcinoma. US Gastroenterol Hepatol Rev. 2011;7(1):59–64.PubMedPubMedCentralGoogle Scholar
  7. 7.
    • Torres J, et al. Gastric cancer incidence and mortality is associated with altitude in the mountainous regions of Pacific Latin America. Cancer Causes Control. 2013;24(2):249–56. Describes gastric cancer risk in a high-incidence, high-mortality region of Latin America. PubMedGoogle Scholar
  8. 8.
    Correa P. The gastric precancerous process. Cancer Surv. 1983;2:437–50.Google Scholar
  9. 9.
    •• Falush D, et al. Traces of human migrations in Helicobacter pylori populations. Science. 2003;299(5612):1582–5. Reports on methods used to define modern H. pylori populations in the context of their ancestral gene pools, which are attributable to human migration. PubMedGoogle Scholar
  10. 10.
    Vale F, et al. Dormant phages of Helicobacter pylori reveal distinct populations in Europe. Sci Rep. 2015;5:14333.PubMedPubMedCentralGoogle Scholar
  11. 11.
    Dominguez-Bello M, Blaser M. The human microbiota as a marker for migrations of individuals and populations. Annu Rev Anthropol. 2011;40:451–74.Google Scholar
  12. 12.
    Burkitt MD, Duckworth CA, Williams JM, Pritchard DM. Helicobacter pylori-induced gastric pathology: insights from in vivo and ex vivo models. Dis Model Mech. 2017;10(2):89–104.PubMedPubMedCentralGoogle Scholar
  13. 13.
    Yamaoka Y. Helicobacter pylori typing as a tool for tracking human migration. Clin Microbiol Infect. 2009;9:829–34.Google Scholar
  14. 14.
    Pallen MJ, Wren BW. Bacterial pathogenomics. Nature. 2007;449:835–42.  https://doi.org/10.1038/nature06248.CrossRefPubMedGoogle Scholar
  15. 15.
    Ciesielski TH. Diverse convergent evidence in the genetic analysis of complex disease: coordinating omic, informatic, and experimental evidence to better identify and validate risk factors. BioData Min. 2014;7:10.PubMedPubMedCentralGoogle Scholar
  16. 16.
    Castro L, Vaz CL. Helicobacter pylori in South America. Can J Gastroenterol. 1998;12(7):509–12.Google Scholar
  17. 17.
    Correa P. A human model of gastric carcinogenesis. Cancer Res. 1988;48(13):3554–60.PubMedGoogle Scholar
  18. 18.
    Peek RM Jr, Blaser MJ. Helicobacter pylori and gastrointestinal tract adenocarcinomas. Nat Rev Cancer. 2002;2(1):28–37.PubMedGoogle Scholar
  19. 19.
    Zhang X, et al. Endoscopic screening in Asian countries is associated with reduced gastric cancer mortality: a meta-analysis and systematic review. Gastroenterology. 2018;155(2):347–54.PubMedGoogle Scholar
  20. 20.
    •• Correa P. Human gastric carcinogenesis: a multistep and multifactorial process–First American Cancer Society award lecture on cancer epidemiology and prevention. Cancer Res. 1992;52(24):6735–40 This is the original characterization of how gastric disease progresses. PubMedGoogle Scholar
  21. 21.
    Mera R, et al. Dynamics of Helicobacter pylori infection as a determinant of progression of gastric precancerous lesions: 16-year follow-up of an eradication trial. Gut. 2017;67(7):1239–46.PubMedGoogle Scholar
  22. 22.
    Chiba T, Seno H, Marusawa H, Wakatsuki Y, Okazaki K. Host factors are important in determining clinical outcomes of Helicobacter pylori infection. J Gastroenterol. 2006;41(1):1–9.PubMedGoogle Scholar
  23. 23.
    Ford A, Forman D, Hunt R, Yuan Y, Moayyedi P. Helicobacter pylori eradication for the prevention of gastric neoplasia. Cochrane Database Syst Rev. 2015;7:CD005583.Google Scholar
  24. 24.
    Ford AC, Forman D, Hunt RH, Yuan Y, Moayyedi P. Helicobacter pylori eradication therapy to prevent gastric cancer in healthy asymptomatic infected individuals: systematic review and meta-analysis of randomized controlled trials. BMJ. 2014;348:g3174.PubMedPubMedCentralGoogle Scholar
  25. 25.
    Abnet CC, et al. A shared susceptibility locus in PLCE1 at 10q23 for gastric adenocarcinoma and esophageal squamous cell carcinoma. Nat Genet. 2010;42:764–7.PubMedPubMedCentralGoogle Scholar
  26. 26.
    Wang LD, et al. Genome-wide association study of esophageal squamous cell carcinoma in Chinese subjects identifies susceptibility loci at PLCE1 and C20orf54. Nat Genet. 2010;42(9):759–63.PubMedGoogle Scholar
  27. 27.
    Engel LS, et al. Population attributable risks of esophageal and gastric cancers. J Natl Cancer Inst. 2003;95(18):1404–13.PubMedGoogle Scholar
  28. 28.
    Vaezi MF, et al. CagA-positive strains of Helicobacter pylori may protect against Barrett’s esophagus. Am J Gastroenterol. 2000;95(9):2206–11.PubMedGoogle Scholar
  29. 29.
    Blaser MJ, Chen Y, Reibman J. Does Helicobacter pylori protect against asthma and allergy? Gut. 2008;57(5):561–7.PubMedPubMedCentralGoogle Scholar
  30. 30.
    •• Kodaman N, et al. Human and Helicobacter pylori coevolution shapes the risk of gastric disease. Proc Natl Acad Sci U S A. 2014;111:1455–60. This is the first study to demonstrate that the interaction between host and H. pylori ancestries completely account for severity of gastric lesions. PubMedPubMedCentralGoogle Scholar
  31. 31.
    • Lunet N, Barros H. Helicobacter pylori infection and gastric cancer: facing the enigmas. Int J Cancer. 2003;106(6):953–60. Demonstrates that H. pylori prevalence does not correlate with incidence of gastric disease and that factors beyond mere geographical location must determine gastric cancer risk. PubMedGoogle Scholar
  32. 32.
    Perez-Perez GI, Rothenbacher D, Brenner H. Epidemiology of Helicobacter pylori infection. Helicobacter. 2004;9(Suppl 1):1–6.PubMedGoogle Scholar
  33. 33.
    Holcombe C. Helicobacter pylori: the African enigma. Gut. 1992;33(4):429–31.PubMedPubMedCentralGoogle Scholar
  34. 34.
    Bravo LE, van Doom LJ, Realpe JL, Correa P. Virulence-associated genotypes of Helicobacter pylori: do they explain the African enigma? Am J Gastroenterol. 2002;97(11):2839–42.PubMedGoogle Scholar
  35. 35.
    Campbell DI, et al. The African enigma: Low prevalence of gastric atrophy, high prevalence of chronic inflammation in West African adults and children. Helicobacter. 2001;6(4):263–7.PubMedGoogle Scholar
  36. 36.
    Ghoshal UC, Chaturvedi R, Correa P. The enigma of Helicobacter pylori infection and gastric cancer. Indian J Gastroenterol. 2010;29(3):95–100.PubMedPubMedCentralGoogle Scholar
  37. 37.
    Román-Román A, et al. Helicobacter pylori vacA s1 m1 genotype but not cagA or babA2 increase the risk of ulcer and gastric cancer in patients from Southern Mexico. Gut Pathog. 2017;9:18.PubMedPubMedCentralGoogle Scholar
  38. 38.
    Cover T. Helicobacter pylori diversity and gastric cancer risk. MBio. 2016;7(1):e01869–15.PubMedPubMedCentralGoogle Scholar
  39. 39.
    Noto JM, Peek RM Jr. The Helicobacter pylori cag pathogenicity Island. Methods Mol Biol. 2012;921:41–50.PubMedPubMedCentralGoogle Scholar
  40. 40.
    Tummuru MKR, 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(5):1799–809.PubMedPubMedCentralGoogle Scholar
  41. 41.
    Covacci A, et al. Molecular characterization of the 128-kDa immunodominant antigen of Helicobacter pylori associated with cytotoxicity and duodenal ulcer. Proc Natl Acad Sci U S A. 1993;90(12):5791–5.PubMedPubMedCentralGoogle Scholar
  42. 42.
    Blaser MJ, et al. 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.PubMedGoogle Scholar
  43. 43.
    Atherton JC, Cao P, Peek RM. Mosaicism in vacuolating cytotoxin alleles of Helicobacter pylori. Association of specific vacA types with cytotoxin production and peptic ulceration. J Biol Chem. 1995;270:17771–17,777.PubMedGoogle Scholar
  44. 44.
    Baldari CT, Lanzavecchia A, Telford JL. Immune subversion by Helicobacter pylori. Trends Immunol. 2005;26(4):199–207.PubMedGoogle Scholar
  45. 45.
    Atherton JC, et al. Vacuolating Cytotoxin (vacA) alleles of helicobacter pylori comprise two geographically widespread types, m1 and m2, and have evolved through limited recombination. Curr Microbiol. 1999;39(4):211–8.PubMedPubMedCentralGoogle Scholar
  46. 46.
    Olbermann P, et al. A global overview of the genetic and functional diversity in the Helicobacter pylori cag pathogenicity island. PLoS Genet. 2010;6(8):e1001069.PubMedPubMedCentralGoogle Scholar
  47. 47.
    Hatakeyama M. Anthropological and clinical implications for the structural diversity of the Helicobacter pylori CagA oncoprotein. Cancer Sci. 2011;102(1):36–43.PubMedGoogle Scholar
  48. 48.
    Suerbaum S, et al. Free recombination within Helicobacter pylori. Proc Natl Acad Sci U S A. 1998;95(21):12619–12,624.PubMedPubMedCentralGoogle Scholar
  49. 49.
    Lichtenstein P, et al. Environmental and heritable factors in the causation of cancer--analyses of cohorts of twins from Sweden, Denmark, and Finland. N Engl J Med. 2000;343(2):78–85.PubMedGoogle Scholar
  50. 50.
    Schneider BG, et al. Cytokine polymorphisms and gastric cancer risk: an evolving view. Cancer Biol Ther. 2008;7(2):157–62.PubMedGoogle Scholar
  51. 51.
    Tang Y, Zhu J, Chen L, Zhang S, Lin J. Associations of matrix metalloproteinase-9 protein polymorphisms with lymph node metastasis but not invasion of gastric cancer. Clin Cancer Res. 2008;14:2870–7.PubMedGoogle Scholar
  52. 52.
    Song HR, et al. Genetic variations in the PRKAA1 and ZBTB20 genes and gastric cancer susceptibility in a Korean population. Mol Carcinog. 2013;52(Suppl 1):E155–60.PubMedGoogle Scholar
  53. 53.
    Garcia-Gonzalez MA, et al. Association of PSCA rs2294008 gene variants with poor prognosis and increased susceptibility to gastric cancer and decreased risk of duodenal ulcer disease. Int J Cancer. 2015;137:1362–73.PubMedGoogle Scholar
  54. 54.
    Sakamoto H, et al. Genetic variation in PSCA is associated with susceptibility to diffuse-type gastric cancer. Nat Genet. 2008;40:730–40.PubMedGoogle Scholar
  55. 55.
    Wang Z, et al. Identification of new susceptibility loci for gastric non-cardia adenocarcinoma: pooled results from two Chinese genome-wide association studies. Gut. 2017;66(4):581–587.PubMedPubMedCentralGoogle Scholar
  56. 56.
    • El-Omar EM, et al. Interleukin-1 polymorphisms associated with increased risk of gastric cancer. Nature. 2000;404:398–402. This is a high quality study where pro-inflammatory cytokine genotypes associated with gastric cancer risk, in the setting of H. pylori infection. PubMedGoogle Scholar
  57. 57.
    El-Omar EM, et al. Increased risk of noncardia gastric cancer associated with proinflammatory cytokine gene polymorphisms. Gastroenterology. 2003;124:1193–201.PubMedGoogle Scholar
  58. 58.
    • Persson C, Canedo P, Machado JC, El-Omar EM, Forman D. Polymorphisms in inflammatory response genes and their association with gastric cancer: a HuGE systematic review and meta-analyses. Am J Epidemiol. 2011;173:259–70. A high quality study that assesses SNPs associated with gastric disease risk in Asian versus non-Asian populations. PubMedGoogle Scholar
  59. 59.
    Mocellin S, Verdi D, Pooley KA, Nitti D. Genetic variation and gastric cancer risk: a field synopsis and meta-analysis. Gut. 2015;64(8):1209–19.PubMedGoogle Scholar
  60. 60.
    Hill AV. The genomics and genetics of human infectious disease susceptibility. Annu Rev Genomics Hum Genet. 2001;2:373–400.  https://doi.org/10.1146/annurev.genom.2.1.373.CrossRefPubMedGoogle Scholar
  61. 61.
    Jallow M, et al. Genome-wide and fine-resolution association analysis of malaria in West Africa. Nat Genet. 2009;41(6):657–65.PubMedPubMedCentralGoogle Scholar
  62. 62.
    Ko DC, Urban TJ. Understanding human variation in infectious disease susceptibility through clinical and cellular GWAS. PLoS Pathog. 2013;9(8):e1003424.PubMedPubMedCentralGoogle Scholar
  63. 63.
    Hill AV. Evolution, revolution and heresy in the genetics of infectious disease susceptibility. Philos Trans R Soc Lond Ser B Biol Sci. 2012;367(1590):840–9.Google Scholar
  64. 64.
    Shi Y, et al. A genome-wide association study identifies new susceptibility loci for non-cardia gastric cancer at 3q13.31 and 5p13.1. Nat Genet. 2011;43:1215–8.PubMedGoogle Scholar
  65. 65.
    Mayerle J, et al. Identification of genetic loci associated with Helicobacter pylori serologic status. JAMA. 2013;309(18):1912–20.PubMedGoogle Scholar
  66. 66.
    El-Omar EM. Helicobacter pylori susceptibility in the GWAS era. JAMA. 2013;309(18):1939–40.PubMedGoogle Scholar
  67. 67.
    Sobota R, et al. Epigenetic and genetic variation in GATA5 is associated with gastric disease risk. Hum Genet. 2016;135(8):895–906.PubMedPubMedCentralGoogle Scholar
  68. 68.
    Teschendorff AE, et al. Age-dependent DNA methylation of genes that are suppressed in stem cells is a hallmark of cancer. Genome Res. 2010;20:440–6.PubMedPubMedCentralGoogle Scholar
  69. 69.
    Schneider BG, et al. DNA methylation predicts progression of human gastric lesions. Cancer Epidemiol Biomark Prev. 2015;24:1607–13.Google Scholar
  70. 70.
    Watanabe Y, et al. Sensitive and specific detection of early gastric cancer with DNA methylation analysis of gastric washes. Gastroenterology. 2009;136:2149–58.PubMedPubMedCentralGoogle Scholar
  71. 71.
    Kupfer S. Gaining ground in the genetics of gastric cancer. Gastroenterology. 2017;152:926–46.PubMedGoogle Scholar
  72. 72.
    van der Post RS, et al. Hereditary diffuse gastric cancer: updated clinical guidelines with an emphasis on germline CDH1 mutation carriers. J Med Genet. 2015;52(6):361–74.PubMedPubMedCentralGoogle Scholar
  73. 73.
    The Cancer Genome Atlas Research Network. Comprehensive molecular characterization of gastric adenocarcinoma. Nature. 2014;513:202–9.Google Scholar
  74. 74.
    Haley KP, Gaddy JA. Nutrition and Helicobacter pylori: host diet and nutritional immunity influence bacterial virulence and disease outcome. Gastroenterol Res Pract. 2016;2016:3019362.PubMedPubMedCentralGoogle Scholar
  75. 75.
    Jakszyn P, et al. Endogenous versus exogenous exposure to N-nitroso compounds and gastric cancer risk in the European Prospective Investigation into Cancer and Nutrition (EPIC-EURGAST) study. Carcinogenesis. 2006;27:1497–501.PubMedGoogle Scholar
  76. 76.
    La Torre G, et al. Smoking status and gastric cancer risk: an updated meta-analysis of case-control studies published in the past ten years. Tumori. 2009;95:13–22.PubMedGoogle Scholar
  77. 77.
    Bonder MJ, et al. The effect of host genetics on the gut microbiome. Nat Genet. 2016;48:1407–12.PubMedGoogle Scholar
  78. 78.
    Kurilshikov A, Wijmenga C, Fu J, Zhernakova A. Host genetics and gut microbiome: challenges and perspectives. Trends Immunol. 2017;38(9):633–647.PubMedGoogle Scholar
  79. 79.
    Kolde R, et al. Host genetic variation and its microbiome interactions within the Human Microbiome Project. BMC Gen Med. 2018;10:6.Google Scholar
  80. 80.
    Wang J, et al. Analysis of intestinal microbiota in hybrid house mice reveals evolutionary divergence in a vertebrate hologenome. Nat Commun. 2015;6:6440.PubMedPubMedCentralGoogle Scholar
  81. 81.
    Guglielmi G. How gut microbes are joining the fight against cancer. Nature (News Features). 2018;55:482–4.Google Scholar
  82. 82.
    Klymiuk I, et al. The human gastric microbiome is predicated upon infection with helicobacter pylori. Front Microbiol. 2017;8:2508.PubMedPubMedCentralGoogle Scholar
  83. 83.
    Thorell K, et al. In vivo analysis of the viable microbiota and helicobacter pylori transcriptome in gastric infection and early stages of carcinogenesis. Infect Immun. 2017;85(10):e00031–17.PubMedPubMedCentralGoogle Scholar
  84. 84.
    • Noto J, Peek R. The gastric microbiome, its interaction with Helicobacter pylori, and its potential role in the progression to stomach cancer. PLoS Pathog. 2017;13(10):e1006573. This describes some potential drivers of gastric cancer susceptibility, within the complex milieu of the human gastric microbiota. PubMedPubMedCentralGoogle Scholar
  85. 85.
    Dicksved J, et al. Molecular characterization of the stomach microbiota in patients with gastric cancer and in controls. J Med Microbiol. 2009;58:509–16.PubMedGoogle Scholar
  86. 86.
    Rothschild D, et al. Environment dominates over host genetics in shaping human gut microbiota. Nature. 2018;55:210–5.Google Scholar
  87. 87.
    •• Linz B, et al. An African origin for the intimate association between humans and Helicobacter pylori. Nature. 2007;445(7130):915–8. Study using sequences from large H. pylori dataset describes genetic diversity in H. pylori decreasing with geographic distance from East Africa, from where H. pylori spread around 58,000 years ago, via human migration. PubMedPubMedCentralGoogle Scholar
  88. 88.
    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(7):674–9.PubMedGoogle Scholar
  89. 89.
    Anderson RM, May RM. Coevolution of hosts and parasites. Parasitology. 1982;85(Pt 2):411–26.PubMedGoogle Scholar
  90. 90.
    Frank SA. Models of parasite virulence. Q Rev Biol. 1996;71(1):37–78.PubMedGoogle Scholar
  91. 91.
    Messenger SL, Molineux IJ, Bull JJ. Virulence evolution in a virus obeys a trade-off. Proc Biol Sci. 1999;266(1417):397–404.PubMedPubMedCentralGoogle Scholar
  92. 92.
    Schwarz S, et al. Horizontal versus familial transmission of Helicobacter pylori. PLoS Pathog. 2008;4(10):e1000180.PubMedPubMedCentralGoogle Scholar
  93. 93.
    Agnew P, Koella JC. Virulence, parasite mode of transmission, and host fluctuating asymmetry. Proc Biol Sci. 1997;264(1378):9–15.PubMedPubMedCentralGoogle Scholar
  94. 94.
    Bull JJ, Molineux IJ, Rice WR. Selection of benevolence in a host-parasite system. Evolution. 1991;45(4):875–82.PubMedGoogle Scholar
  95. 95.
    Carroll IM, Khan AA, Ahmed N. Revisiting the pestilence of Helicobacter pylori: Insights into geographical genomics and pathogen evolution. Infect Genet Evol. 2004;4(2):81–90.PubMedGoogle Scholar
  96. 96.
    Ansari S, Yamaoka Y. Helicobacter pylori BabA in adaptation for gastric colonization. World J Gastroenterol. 2017;23(23):4158–69.PubMedPubMedCentralGoogle Scholar
  97. 97.
    • Kodaman N, Sobota RS, Mera R, Schneider BG, Williams SM. Disrupted human-pathogen co-evolution: a model for disease. Front Genet. 2014;5:290. Describes a disrupted co-evolution model between host and pathogen, and the need to study genome-by-genome interactions, to explain disease outcome variation, in the context of multiple infectious diseases. PubMedPubMedCentralGoogle Scholar
  98. 98.
    Pazos A, et al. Draft genome sequences of 13 Colombian Helicobacter pylori strains isolated from Pacific Coast and Andean residents. Genome Announc. 2017;5(15):e00113–7.PubMedPubMedCentralGoogle Scholar
  99. 99.
    Moreno-Estrada A, et al. Reconstructing the population genetic history of the Caribbean. PLoS Genet. 2013;9(11):e1003925.PubMedPubMedCentralGoogle Scholar
  100. 100.
    Correa P, et al. Gastric cancer in Colombia. III. Natural history of precursor lesions. J Natl Cancer Inst. 1976;57(5):1027–35.PubMedGoogle Scholar
  101. 101.
    Moodley Y, et al. Age of the association between Helicobacter pylori and man. PLoS Pathog. 2012;8(5):e1002693.PubMedPubMedCentralGoogle Scholar
  102. 102.
    Thompson JN, Nuismer SL, Gomulkiewicz R. Coevolution and maladaptation. Integr Comp Biol. 2002;42(2):381–7.PubMedGoogle Scholar
  103. 103.
    Cochran GM, Ewald PW, Cochran KD. Infectious causation of disease: an evolutionary perspective. Perspect Biol Med. 2000;43(3):406–48.PubMedGoogle Scholar
  104. 104.
    Ghose C, Perez-Perez GI, van Doorn LJ, Domínguez-Bello MG, Blaser MJ. High frequency of gastric colonization with multiple Helicobacter pylori strains in Venezuelan subjects. J Clin Microbiol. 2005;43(6):2635–41.PubMedPubMedCentralGoogle Scholar
  105. 105.
    Moodley Y, et al. The peopling of the Pacific from a bacterial perspective. Science. 2009;323(5913):527–30.PubMedPubMedCentralGoogle Scholar
  106. 106.
    Wirth T, et al. Distinguishing human ethnic groups by means of sequences from Helicobacter pylori: lessons from Ladakh. Proc Natl Acad Sci U S A. 2004;101(14):4746–51.PubMedPubMedCentralGoogle Scholar
  107. 107.
    Latifi-Navid S, et al. Ethnic and geographic differentiation of Helicobacter pylori within Iran. PLoS ONE. 2010;5(3):e9645.PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2018

Authors and Affiliations

  • Gloria Tavera
    • 1
  • Douglas R. Morgan
    • 2
    • 3
  • Scott M. Williams
    • 1
  1. 1.Department of Population and Quantitative Health SciencesCase Western Reserve UniversityClevelandUSA
  2. 2.Vanderbilt Ingram Cancer CenterNashvilleUSA
  3. 3.Division of Gastroenterology, Hepatology, and Nutrition, Department of MedicineVanderbilt University Medical CenterNashvilleUSA

Personalised recommendations