1887

Abstract

, a Gram-negative bacterium, is a causal agent of peptic ulcers and is estimated to infect the gastric mucosa of at least half of the world's population. As primary infections are acquired mainly by household contact, studies on family clusters provide a model for investigating transmission and the natural history of initial infection. Here, sequence typing exploiting genetic variation in core fragments of three key housekeeping loci (, and ) was used to determine clonal descent amongst isolates of ten members of four families in Northern Ireland and a family with three generations in central England. Phylogenetic analysis of each locus for 73 strains of from 11 countries indicated high background intraspecific diversity, apart from identical paired isolates from five unrelated patients and strains with identical sequence types (STs) detected in adult members of two families. In several families carrying strains with different STs, evidence of residual clonal descent was detected at one or two loci by comparison of nucleotide and amino acid sequences. Pathogenicity-associated genotypes were heterogeneous with respect to ST and amino acid type. Analysis of these three housekeeping genes provides unique evidence for precise tracing of clonal descent in isolates of in family groups.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.04988-0
2003-06-01
2020-01-24
Loading full text...

Full text loading...

/deliver/fulltext/jmm/52/6/JM520612.html?itemId=/content/journal/jmm/10.1099/jmm.0.04988-0&mimeType=html&fmt=ahah

References

  1. Achtman, M., Azuma, T., Berg, D. E. & 7 other authors ( 1999;). Recombination and clonal groupings within Helicobacter pylori from different geographical regions. Mol Microbiol 32, 459–470.[CrossRef]
    [Google Scholar]
  2. Alm, R. A., Ling, L. S., Moir, D. T. & 20 other authors ( 1999;). Genomic-sequence comparison of two unrelated isolates of the human gastric pathogen Helicobacter pylori. Nature 397, 176–180.[CrossRef]
    [Google Scholar]
  3. Atherton, J. C., Cover, T. L., Twells, R. J., Morales, M. R., Hawkey, C. J. & Blaser, M. J. ( 1999;). Simple and accurate PCR-based system for typing vacuolating cytotoxin alleles of Helicobacter pylori. J Clin Microbiol 37, 2979–2982.
    [Google Scholar]
  4. Bamford, K. B., Bickley, J., Collins, J. S., Johnston, B. T., Potts, S., Boston, V., Owen, R. J. & Sloan, J. M. ( 1993;). Helicobacter pylori: comparison of DNA fingerprints provides evidence for intrafamilial infection. Gut 34, 1348–1350.[CrossRef]
    [Google Scholar]
  5. Brenner, H., Rothenbacher, D., Bode, G. & Adler, G. ( 1998;). Parental history of gastric or duodenal ulcer and prevalence of Helicobacter pylori infection in preschool children: population based study. BMJ 316, 665. 665.[CrossRef]
    [Google Scholar]
  6. Brenner, H., Rothenbacher, D., Bode, G., Dieudonne, P. & Adler, G. ( 1999;). Active infection with Helicobacter pylori in healthy couples. Epidemiol Infect 122, 91–95.[CrossRef]
    [Google Scholar]
  7. Brown, L. M. ( 2000;). Helicobacter pylori: epidemiology and routes of transmission. Epidemiol Rev 22, 283–297.[CrossRef]
    [Google Scholar]
  8. Calam, J. & Baron, J. H. ( 2001;). ABC of the upper gastrointestinal tract: pathophysiology of duodenal and gastric ulcer and gastric cancer. BMJ 323, 980–982.[CrossRef]
    [Google Scholar]
  9. Chalkaukas, H., Kersulyte, D., Cepuliene, I., Urbonas, V., Ruzeviciene, D., Barakauskiene, A., Raudonikiene, A. & Berg, D. E. ( 1998;). Genotypes of Helicobacter pylori in Lithuanian families. Helicobacter 3, 296–302.
    [Google Scholar]
  10. Dominici, P., Bellentani, S., Di Biase, A. R. & 9 other authors ( 1999;). Familial clustering of Helicobacter pylori infection: population based study. BMJ 319, 537–540.[CrossRef]
    [Google Scholar]
  11. Drumm, B., Perez-Perez, G. I., Blaser, M. J. & Sherman, P. M. ( 1990;). Intrafamilial clustering of Helicobacter pylori infection. N Engl J Med 322, 359–363.[CrossRef]
    [Google Scholar]
  12. Dunn, B. E., Cohen, H. & Blaser, M. J. ( 1997;). Helicobacter pylori. Clin Microbiol Rev 10, 720–741.
    [Google Scholar]
  13. Enright, M. C. & Spratt, B. G. ( 1999;). Multilocus sequence typing. Trends Microbiol 7, 482–487.[CrossRef]
    [Google Scholar]
  14. Falush, D., Kraft, C., Taylor, N. S., Correa, P., Fox, J. G., Achtman, M. & Suerbaum, S. ( 2001;). Recombination and mutation during long-term gastric colonization by Helicobacter pylori: estimates of clock rates, recombination size, and minimal age. Proc Natl Acad Sci U S A 98, 15056–15061.[CrossRef]
    [Google Scholar]
  15. Feldman, R. A. ( 2001;). Epidemiologic observations and open questions about disease and infection caused by Helicobacter pylori. In Helicobacter pylori: Molecular and Cellular Biology, pp. 29–51. Edited by M. Achtman & S. Suerbaum. Wymondham: Horizon.
  16. Georgopoulos, S. D., Mentis, A. F., Spiliadis, C. A., Tzouvelekis, L. S., Tzelepi, E., Moshopoulos, A. & Skandalis, N. ( 1996;). Helicobacter pylori infection in spouses of patients with duodenal ulcers and comparison of ribosomal RNA gene patterns. Gut 39, 634–638.[CrossRef]
    [Google Scholar]
  17. Goodman, K. J. & Correa, P. ( 2000;). Transmission of Helicobacter pylori among siblings. Lancet 355, 358–362.[CrossRef]
    [Google Scholar]
  18. Hall, T. A. ( 1999;). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41, 95–98.
    [Google Scholar]
  19. Han, S.-R., Zschausch, H.-C. E., Meyer, H.-G. W., Schneider, T., Loos, M., Bhakdi, S. & Maeurer, M. J. ( 2000;). Helicobacter pylori: clonal population structure and restricted transmission within families revealed by molecular typing. J Clin Microbiol 38, 3646–3651.
    [Google Scholar]
  20. Israel, D. A., Salama, N., Krishna, U., Rieger, U. M., Atherton, J. C., Falkow, S. & Peek, R. M., Jr ( 2001;). Helicobacter pylori genetic diversity within the gastric niche of a single human host. Proc Natl Acad Sci U S A 98, 14625–14630.[CrossRef]
    [Google Scholar]
  21. Kelly, D. J., Hughs, N. J. & Poole, R. K. ( 2001;). Microaerobic physiology: aerobic respiration, anaerobic respiration and carbon dioxide metabolism. In Helicobacter pylori: Physiology and Genetics, pp. 113–133. Edited by H. L. T. Mobley, G. L. Mendz & S. L. Hazell. Washington, DC: American Society for Microbiology.
  22. Kuo, C.-H., Poon, S.-K., Su, Y.-C., Su, R., Chang, C.-S. & Wang, W.-C. ( 1999;). Heterogeneous Helicobacter pylori isolates from H.pylori-infected couples in Taiwan. J Infect Dis 180, 2064–2068.[CrossRef]
    [Google Scholar]
  23. Lee, A., O'Rourke, J., De Ungria, M. C., Robertson, B., Daskalopoulos, G. & Dixon, M. F. ( 1997;). A standardized mouse model of Helicobacter pylori infection: introducing the Sydney strain. Gastroenterology 112, 1386–1397.[CrossRef]
    [Google Scholar]
  24. Lundstrom, A. M., Sundaeus, V. & Bolin, I. ( 2001;). The 26-kilodalton, AhpC homologue, of Helicobacter pylori is also produced by other Helicobacter species. Helicobacter 6, 44–54.[CrossRef]
    [Google Scholar]
  25. Maggi Solcà, N., Bernasconi M. V., Valsangiacomo, C., Van Doorn, L.-J. & Piffaretti, J.-C. ( 2001;). Population genetics of Helicobacter pylori in the southern part of Switzerland analysed by sequencing of four housekeeping genes (atpD, glnA, scoB and recA), and by vacA, cagA, iceA and IS605 genotyping. Microbiology 147, 1693–1707.
    [Google Scholar]
  26. Malaty, H. M., Graham, D. Y. & Klein, P. D., Evans, D. G., Adam, E. & Evans, D. J. ( 1991;). Transmission of Helicobacter pylori infection.Studies in families of healthy individuals. Scand J Gastroenterol 26, 927–932.[CrossRef]
    [Google Scholar]
  27. Malaty, H. M., Kumagai, T., Tanaka, E., Ota, H., Kiyosawa, K., Graham, D. Y. & Katsuyama, T. ( 2000;). Evidence from a nine-year birth cohort study in Japan of transmission pathways of Helicobacter pylori infection. J Clin Microbiol 38, 1971–1973.
    [Google Scholar]
  28. Malaty, H. M., El-Kasabany, A., Graham, D. Y., Miller, C. C., Reddy, S. G., Srinivasan, S. R., Yamaoka, Y. & Berenson, G. S. ( 2002;). Age at acquisition of Helicobacter pylori infection: a follow-up study from infancy to adulthood. Lancet 359, 931–935.[CrossRef]
    [Google Scholar]
  29. McAtee, C. P., Hoffman, P. S. & Berg, D. E. ( 2001;). Identification of differentially regulated proteins in metronidozole resistant Helicobacter pylori by proteome techniques. Proteomics 1, 516–521.[CrossRef]
    [Google Scholar]
  30. Mendall, M. A., Goggin, P. M., Molineaux, N., Levy, J., Toosy, T., Strachan, D. & Northfield, T. C. ( 1992;). Childhood living conditions and Helicobacter pylori seropositivity in adult life. Lancet 339, 896–897.[CrossRef]
    [Google Scholar]
  31. Mobley, H. L. T. ( 2001;). Urease. In Helicobacter pylori: Physiology and Genetics, pp. 179–191. Edited by H. L. T. Mobley, G. L. Mendz & S. L. Hazell. Washington, DC: American Society for Microbiology.
  32. Ng, B. L., Ng, H. C., Goh, K. T. & Ho, B. ( 2001;). Helicobacter pylori in familial clusters based on antibody profile. FEMS Immunol Med Microbiol 30, 139–142.[CrossRef]
    [Google Scholar]
  33. Nwokolo, C. U., Bickley, J., Attard, A. R., Owen, R. J., Costas, M. & Fraser, I. A. ( 1992;). Evidence of clonal variants of Helicobacter pylori in three generations of a duodenal ulcer disease family. Gut 33, 1323–1327.[CrossRef]
    [Google Scholar]
  34. Oderda, G., Vaira, D., Holton, J., Ainley, C., Altare, F., Boero, M., Smith, A. & Ansaldi, N. ( 1991;). Helicobacter pylori in children with peptic ulcer and their families. Dig Dis Sci 36, 572–576.[CrossRef]
    [Google Scholar]
  35. Owen, R. J. ( 1993;). Microbiological aspects of Helicobacter pylori infection. Commun Dis Rep CDR Rev 3, R51–56.
    [Google Scholar]
  36. Owen, R. J., Slater, E. R., Gibson, J., Lorenz, E. & Tompkins, D. S. ( 1999;). Effect of clarithromycin and omeprazole therapy on the diversity and stability of genotypes of Helicobacter pylori from duodenal ulcer patients. Microb Drug Resist 5, 141–146.[CrossRef]
    [Google Scholar]
  37. Owen, R. J., Peters, T. M., Varea, R., Teare, E. L. & Saverymuttu, S. ( 2001a;). Molecular epidemiology of Helicobacter pylori in England: prevalence of cag pathogenicity island markers and IS605 presence in relation to patient age and severity of gastric disease. FEMS Immunol Med Microbiol 30, 65–71.[CrossRef]
    [Google Scholar]
  38. Owen, R. J., Taylor, D. E., Wang, G. & Van Doorn, L.-J. ( 2001b;). Heterogeneity and subtyping. In Helicobacter pylori: Physiology and Genetics, pp. 343–378. Edited by H. L. T. Mobley, G. L. Mendz & S. L. Hazell. Washington, DC: American Society for Microbiology.
  39. Owen, R. J., Xerry, J. & Chisholm, S. A. ( 2001c;). Sequence diversity within the Helicobacter pylori ureI locus and identification of homologues in other species of Helicobacter of human and animal origin. Gut 49 (Suppl. 11), A9. A9.[CrossRef]
    [Google Scholar]
  40. Pounder, R. E. & Ng, D. ( 1995;). The prevalence of Helicobacter pylori infection in different countries. Aliment Pharmacol Ther 9 (Suppl. 2), 33–39.
    [Google Scholar]
  41. Rothenbacher, D., Bode, G., Berg, G., Knayer, U., Gonser, T., Adler, G. & Brenner, H. ( 1999;). Helicobacter pylori among preschool children and their parents: evidence of parent-child transmission. J Infect Dis 179, 398–402.[CrossRef]
    [Google Scholar]
  42. Rothenbacher, D., Bode, G. & Brenner, H. ( 2000;). Helicobacter pylori among siblings. Lancet 355, 1998. 1998.[CrossRef]
    [Google Scholar]
  43. Rowland, M. ( 2000;). Transmission of Helicobacter pylori: is it all child's play? Lancet 355, 332–333.[CrossRef]
    [Google Scholar]
  44. Saitou, N. & Nei, M. ( 1987;). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406–425.
    [Google Scholar]
  45. Singh, V., Trikha, B., Vaiphei, K. Nain, C. K., Thennarasu, K. & Singh, K. ( 1999;). Helicobacter pylori: evidence for spouse-to-spouse transmission. J Gastroenterol Hepatol 14, 519–522.
    [Google Scholar]
  46. Slater, E., Owen, R. J, Williams, M. & Pounder, R. E. ( 1999;). Conservation of the cag pathogenicity island of Helicobacter pylori: associations with vacuolating cytotoxin allele and IS605 diversity. Gastroenterology 117, 1308–1315.[CrossRef]
    [Google Scholar]
  47. Stone, M. A., Taub, N., Barnett, D. B. & Mayberry, J. F. ( 2000;). Increased risk of infection with Helicobacter pylori in spouses of infected subjects: observations in a general population sample from the UK. Hepatogastroenterology 47, 433–436.
    [Google Scholar]
  48. Suerbaum, S., Smith, J. M., Bapumia, K., Morelli, G., Smith, N. H., Kunstmann, E., Dyrek, I. & Achtman, M. ( 1998;). Free recombination within Helicobacter pylori. Proc Natl Acad Sci U S A 95, 12619–12624.[CrossRef]
    [Google Scholar]
  49. Suerbaum, S., Kraft, C., Dewhirst, F. E. & Fox, J. G. ( 2002;). Helicobacter nemestrinae ATCC 49396T is a strain of Helicobacter pylori (Marshall et al.1985) Goodwin et al. 1989, and Helicobacter nemestrinae Bronsdon et al. 1991 is therefore a junior heterotypic synonym of Helicobacter pylori. Int J Syst Evol Microbiol 52, 437–439.
    [Google Scholar]
  50. Suzuki, J., Muraoka, H., Kobayasi, I., Fujita, T. & Mine, T. ( 1999;). Rare incidence of interspousal transmission of Helicobacter pylori in asymptomatic individuals in Japan. J Clin Microbiol 37, 4174–4176.
    [Google Scholar]
  51. Taneike, I., Tamura, Y., Shimizu, T., Yamashiro, Y. & Yamamoto, T. ( 2001;). Helicobacter pylori intrafamilial infections: change in source of infection of a child from father to mother after eradication therapy. Clin Diagn Lab Immunol 8, 731–739.
    [Google Scholar]
  52. Tomb, J. F., White, O., Kerlavage, A. R. & 39 other authors ( 1997;). The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388, 539–547.[CrossRef]
    [Google Scholar]
  53. Van de Peer, Y. & De Wachter, R. ( 1994;). treecon for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. Comput Appl Biosci 10, 569–570.
    [Google Scholar]
  54. van der Ende, A., Rauws, E. A. J., Feller, M., Mulder, C. J., Tytgat, G. N. & Dankert, J. ( 1996;). Heterogeneous Helicobacter pylori isolates from members of a family with a history of peptic ulcer disease. Gastroenterology 111, 638–647.[CrossRef]
    [Google Scholar]
  55. Weeks, D. L., Eskandari, S., Scott, D. R. & Sachs, G. ( 2000;). A H+-gated urea channel: the link between Helicobacter pylori urease and gastric colonization. Science 287, 482–485.[CrossRef]
    [Google Scholar]
  56. Wilson, K. ( 1987;). Preparation of genomic DNA from bacteria. In Current Protocols in Molecular Biology, pp. 2.4.1–2.4.5. Edited by F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. A. Smith, J. G. Seidman & K. Struhl. New York: Wiley.
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.04988-0
Loading
/content/journal/jmm/10.1099/jmm.0.04988-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error